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Chloroplast

Plant organelle that conducts photosynthesis

Science Biological and Health Sciences Cell biology Plant cells

A chloroplast is a plastid organelle primarily responsible for photosynthesis in plant and algal cells. It contains chlorophyll to capture sunlight energy, converting it to chemical energy that fuels the Calvin cycle, producing sugars and organic molecules while releasing oxygen. Chloroplasts also play roles in fatty acid synthesis and amino acid synthesis. Originating from a photosynthetic cyanobacterium engulfed by an early eukaryotic cell, chloroplasts carry their own DNA and must be inherited during cell division. Their presence spans diverse species due to multiple secondary and tertiary endosymbiotic events.

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Discovery and etymology

The first definitive description of a chloroplast (Chlorophyllkörnen, "grain of chlorophyll") was given by Hugo von Mohl in 1837 as discrete bodies within the green plant cell.⁴ In 1883, Andreas Franz Wilhelm Schimper named these bodies as "chloroplastids" (Chloroplastiden).⁵ In 1884, Eduard Strasburger adopted the term "chloroplasts" (Chloroplasten).⁶ ⁷ ⁸

The word chloroplast is derived from the Greek words chloros (χλωρός), which means green, and plastes (πλάστης), which means "the one who forms".⁹

Endosymbiotic origin of chloroplasts

Main article: Plastid evolution

See also: Cyanobacteria and Symbiogenesis

Chloroplasts are one of many types of organelles in photosynthetic eukaryotic cells. They evolved from cyanobacteria through a process called organellogenesis.¹⁰ Cyanobacteria are a diverse phylum of gram-negative bacteria capable of carrying out oxygenic photosynthesis. Like chloroplasts, they have thylakoids.¹¹ The thylakoid membranes contain photosynthetic pigments, including chlorophyll a.¹² ¹³ This origin of chloroplasts was first suggested by the Russian biologist Konstantin Mereschkowski in 1905¹⁴ after Andreas Franz Wilhelm Schimper observed in 1883 that chloroplasts closely resemble cyanobacteria.¹⁵ Chloroplasts are only found in plants, algae,¹⁶ and some species of the amoeboid Paulinella.¹⁷

Mitochondria are thought to have come from a similar endosymbiosis event, where an aerobic prokaryote was engulfed.¹⁸

Primary endosymbiosis

Approximately two billion years ago,¹⁹ ²⁰ ²¹ a free-living cyanobacterium entered an early eukaryotic cell, either as food or as an internal parasite,²² but managed to escape the phagocytic vacuole it was contained in and persist inside the cell.²³ This event is called endosymbiosis, or "cell living inside another cell with a mutual benefit for both". The external cell is commonly referred to as the host while the internal cell is called the endosymbiont.²⁴ The engulfed cyanobacteria provided an advantage to the host by providing sugar from photosynthesis.²⁵ Over time, the cyanobacterium was assimilated, and many of its genes were lost or transferred to the nucleus of the host.²⁶ Some of the cyanobacterial proteins were then synthesized by host cell and imported back into the chloroplast (formerly the cyanobacterium), allowing the host to control the chloroplast.²⁷ ²⁸

Chloroplasts which can be traced back directly to a cyanobacterial ancestor (i.e. without a subsequent endosymbiotic event) are known as primary plastids ("plastid" in this context means almost the same thing as chloroplast²⁹).³⁰ Chloroplasts that can be traced back to another photosynthetic eukaryotic endosymbiont are called secondary plastids or tertiary plastids (discussed below).

Whether primary chloroplasts came from a single endosymbiotic event or multiple independent engulfments across various eukaryotic lineages was long debated. It is now generally held that with one exception (the amoeboid Paulinella chromatophora), chloroplasts arose from a single endosymbiotic event around two billion years ago and these chloroplasts all share a single ancestor.³¹ It has been proposed this the closest living relative of the ancestral engulfed cyanobacterium is Gloeomargarita lithophora.³² ³³ ³⁴ Separately, somewhere about 90–140 million years ago, this process happened again in the amoeboid Paulinella with a cyanobacterium in the genus Prochlorococcus. This independently evolved chloroplast is often called a chromatophore instead of a chloroplast.³⁵ ³⁶

Chloroplasts are believed to have arisen after mitochondria, since all eukaryotes contain mitochondria, but not all have chloroplasts.³⁷ ³⁸ This is called serial endosymbiosis—where an early eukaryote engulfed the mitochondrion ancestor, and then descendants of it then engulfed the chloroplast ancestor, creating a cell with both chloroplasts and mitochondria.³⁹

Secondary and tertiary endosymbiosis

Many other organisms obtained chloroplasts from the primary chloroplast lineages through secondary endosymbiosis—engulfing a red or green alga with a primary chloroplast. These chloroplasts are known as secondary plastids.⁴⁰

As a result of the secondary endosymbiotic event, secondary chloroplasts have additional membranes outside of the original two in primary chloroplasts.⁴¹ In secondary plastids, typically only the chloroplast, and sometimes its cell membrane and nucleus remain, forming a chloroplast with three or four membranes⁴²—the two cyanobacterial membranes, sometimes the eaten alga's cell membrane, and the phagosomal vacuole from the host's cell membrane.⁴³

The genes in the phagocytosed eukaryote's nucleus are often transferred to the secondary host's nucleus.⁴⁴ Cryptomonads and chlorarachniophytes retain the phagocytosed eukaryote's nucleus, an object called a nucleomorph,⁴⁵ located between the second and third membranes of the chloroplast.⁴⁶ ⁴⁷

All secondary chloroplasts come from green and red algae. No secondary chloroplasts from glaucophytes have been observed, probably because glaucophytes are relatively rare in nature, making them less likely to have been taken up by another eukaryote.⁴⁸

Still other organisms, including the dinoflagellates Karlodinium and Karenia, obtained chloroplasts by engulfing an organism with a secondary plastid. These are called tertiary plastids.⁴⁹

Primary chloroplast lineages

All primary chloroplasts belong to one of four chloroplast lineages—the glaucophyte chloroplast lineage, the rhodophyte ("red") chloroplast lineage, and the chloroplastidan ("green") chloroplast lineage, the amoeboid Paulinella chromatophora lineage.⁵⁰ The glaucophyte, rhodophyte, and chloroplastidian lineages are all descended from the same ancestral endosymbiotic event and are all within the group Archaeplastida.⁵¹

Glaucophyte chloroplasts

Rhodophyta (red chloroplasts)

Chloroplastida (green chloroplasts)

Paulinella chromatophora

Secondary and tertiary chloroplast lineages

Green algal derived chloroplasts

Green algae have been taken up by many groups in three or four separate events.⁹³ Primarily, secondary chloroplasts derived from green algae are in the euglenids and chlorarachniophytes. They are also found in one lineage of dinoflagellates ⁹⁴ and possibly the ancestor of the CASH lineage (cryptomonads, alveolates, stramenopiles and haptophytes)⁹⁵ Many green algal derived chloroplasts contain pyrenoids, but unlike chloroplasts in their green algal ancestors, storage product collects in granules outside the chloroplast.⁹⁶

Euglenophytes

Chlorarachniophytes

Prasinophyte-derived chloroplast

Tripartite symbiosis

The ciliate Pseudoblepharisma tenue has two bacterial symbionts, one pink, one green. In 2021, both symbionts were confirmed to be photosynthetic: Ca. Thiodictyon intracellulare (Chromatiaceae), a purple sulfur bacterium with a genome just half the size of their closest known relatives; and Chlorella sp. K10, a green alga.¹¹⁶ There is also a variant of Pseudoblepharisma tenue that only contains chloroplasts from green algae and no endosymbiotic purple bacteria.¹¹⁷

Red algal derived chloroplasts

Secondary chloroplasts derived from red algae appear to have only been taken up only once, which then diversified into a large group called chromists or chromalveolates. Today they are found in the haptophytes, cryptomonads, heterokonts, dinoflagellates and apicomplexans (the CASH lineage).¹¹⁸ Red algal secondary chloroplasts usually contain chlorophyll c and are surrounded by four membranes.¹¹⁹

However, chromist monophyly has been rejected, and it is considered more likely that some chromists acquired their plastids by incorporating another chromist instead of inheriting them from a common ancestor. Cryptophytes seem to have acquired plastids from red algae, which were then transmitted from them to both the Heterokontophytes and the Haptophytes, and then from these last to the Myzozoa.¹²⁰

Cryptophytes

Haptophytes

Stramenopiles (heterokontophytes)

Apicomplexans, chromerids, and dinophytes

Apicomplexans

Apicomplexans are a group of alveolates. Like the helicosproidia, they're parasitic, and have a nonphotosynthetic chloroplast.¹⁴⁰ They were once thought to be related to the helicosproidia, but it is now known that the helicosproida are green algae rather than part of the CASH lineage.¹⁴¹ The apicomplexans include Plasmodium, the malaria parasite. Many apicomplexans keep a vestigial red algal derived chloroplast¹⁴² ¹⁴³ called an apicoplast, which they inherited from their ancestors. Apicoplasts have lost all photosynthetic function, and contain no photosynthetic pigments or true thylakoids. They are bounded by four membranes, but the membranes are not connected to the endoplasmic reticulum.¹⁴⁴ Other apicomplexans like Cryptosporidium have lost the chloroplast completely.¹⁴⁵ Apicomplexans store their energy in amylopectin granules that are located in their cytoplasm, even though they are nonphotosynthetic.¹⁴⁶

The fact that apicomplexans still keep their nonphotosynthetic chloroplast around demonstrates how the chloroplast carries out important functions other than photosynthesis. Plant chloroplasts provide plant cells with many important things besides sugar, and apicoplasts are no different—they synthesize fatty acids, isopentenyl pyrophosphate, iron-sulfur clusters, and carry out part of the heme pathway.¹⁴⁷ The most important apicoplast function is isopentenyl pyrophosphate synthesis—in fact, apicomplexans die when something interferes with this apicoplast function, and when apicomplexans are grown in an isopentenyl pyrophosphate-rich medium, they dump the organelle.¹⁴⁸

Chromerids

The chromerids are a group of algae known from Australian corals which comprise some close photosynthetic relatives of the apicomplexans. The first member, Chromera velia, was discovered and first isolated in 2001. The discovery of Chromera velia with similar structure to the apicomplexans, provides an important link in the evolutionary history of the apicomplexans and dinophytes. Their plastids have four membranes, lack chlorophyll c and use the type II form of RuBisCO obtained from a horizontal transfer event.¹⁴⁹

Dinophytes

The dinoflagellates are yet another very large and diverse group, around half of which are at least partially photosynthetic (i.e. mixotrophic).¹⁵⁰ ¹⁵¹ Dinoflagellate chloroplasts have relatively complex history. Most dinoflagellate chloroplasts are secondary red algal derived chloroplasts. Many dinoflagellates have lost the chloroplast (becoming nonphotosynthetic), some of these have replaced it though tertiary endosymbiosis.¹⁵² Others replaced their original chloroplast with a green algal derived chloroplast.¹⁵³ ¹⁵⁴ ¹⁵⁵ The peridinin chloroplast is thought to be the dinophytes' "original" chloroplast,¹⁵⁶ which has been lost, reduced, replaced, or has company in several other dinophyte lineages.¹⁵⁷

The most common dinophyte chloroplast is the peridinin-type chloroplast, characterized by the carotenoid pigment peridinin in their chloroplasts, along with chlorophyll a and chlorophyll c2.¹⁵⁸ ¹⁵⁹ Peridinin is not found in any other group of chloroplasts.¹⁶⁰ The peridinin chloroplast is bounded by three membranes (occasionally two),¹⁶¹ having lost the red algal endosymbiont's original cell membrane.¹⁶² ¹⁶³ The outermost membrane is not connected to the endoplasmic reticulum.¹⁶⁴ ¹⁶⁵ They contain a pyrenoid, and have triplet-stacked thylakoids. Starch is found outside the chloroplast.¹⁶⁶ Peridinin chloroplasts also have DNA that is highly reduced and fragmented into many small circles.¹⁶⁷ Most of the genome has migrated to the nucleus, and only critical photosynthesis-related genes remain in the chloroplast.

Most dinophyte chloroplasts contain form II RuBisCO, at least the photosynthetic pigments chlorophyll a, chlorophyll c2, beta-carotene, and at least one dinophyte-unique xanthophyll (peridinin, dinoxanthin, or diadinoxanthin), giving many a golden-brown color.¹⁶⁸ ¹⁶⁹ All dinophytes store starch in their cytoplasm, and most have chloroplasts with thylakoids arranged in stacks of three.¹⁷⁰

Haptophyte-derived chloroplasts

The fucoxanthin dinophyte lineages (including Karlodinium and Karenia)¹⁷¹ lost their original red algal derived chloroplast, and replaced it with a new chloroplast derived from a haptophyte endosymbiont, making these tertiary plastids. Karlodinium and Karenia probably took up different endosymbionts.¹⁷² Because the haptophyte chloroplast has four membranes, tertiary endosymbiosis would be expected to create a six membraned chloroplast, adding the haptophyte's cell membrane and the dinophyte's phagosomal vacuole.¹⁷³ However, the haptophyte was heavily reduced, stripped of a few membranes and its nucleus, leaving only its chloroplast (with its original double membrane), and possibly one or two additional membranes around it.¹⁷⁴ ¹⁷⁵

Fucoxanthin-containing chloroplasts are characterized by having the pigment fucoxanthin (actually 19′-hexanoyloxy-fucoxanthin and/or 19′-butanoyloxy-fucoxanthin) and no peridinin. Fucoxanthin is also found in haptophyte chloroplasts, providing evidence of ancestry.¹⁷⁶

Diatom-derived chloroplasts

Some dinophytes, like Kryptoperidinium and Durinskia,¹⁷⁷ have a diatom (heterokontophyte)-derived chloroplast.¹⁷⁸ These chloroplasts are bounded by up to five membranes,¹⁷⁹ (depending on whether the entire diatom endosymbiont is counted as the chloroplast, or just the red algal derived chloroplast inside it). The diatom endosymbiont has been reduced relatively little—it still retains its original mitochondria,¹⁸⁰ and has endoplasmic reticulum, ribosomes, a nucleus, and of course, red algal derived chloroplasts—practically a complete cell,¹⁸¹ all inside the host's endoplasmic reticulum lumen.¹⁸² However the diatom endosymbiont can't store its own food—its storage polysaccharide is found in granules in the dinophyte host's cytoplasm instead.¹⁸³ ¹⁸⁴ The diatom endosymbiont's nucleus is present, but it probably can't be called a nucleomorph because it shows no sign of genome reduction, and might have even been expanded.¹⁸⁵ Diatoms have been engulfed by dinoflagellates at least three times.¹⁸⁶

The diatom endosymbiont is bounded by a single membrane,¹⁸⁷ inside it are chloroplasts with four membranes. Like the diatom endosymbiont's diatom ancestor, the chloroplasts have triplet thylakoids and pyrenoids.¹⁸⁸

In some of these genera, the diatom endosymbiont's chloroplasts aren't the only chloroplasts in the dinophyte. The original three-membraned peridinin chloroplast is still around, converted to an eyespot.¹⁸⁹ ¹⁹⁰

Kleptoplasty

Main article: Kleptoplasty

In some groups of mixotrophic protists, like some dinoflagellates (e.g. Dinophysis), chloroplasts are separated from a captured alga and used temporarily. These klepto chloroplasts may only have a lifetime of a few days and are then replaced.¹⁹¹ ¹⁹²

Cryptophyte-derived dinophyte chloroplast

Members of the genus Dinophysis have a phycobilin-containing¹⁹³ chloroplast taken from a cryptophyte.¹⁹⁴ However, the cryptophyte is not an endosymbiont—only the chloroplast seems to have been taken, and the chloroplast has been stripped of its nucleomorph and outermost two membranes, leaving just a two-membraned chloroplast. Cryptophyte chloroplasts require their nucleomorph to maintain themselves, and Dinophysis species grown in cell culture alone cannot survive, so it is possible (but not confirmed) that the Dinophysis chloroplast is a kleptoplast—if so, Dinophysis chloroplasts wear out and Dinophysis species must continually engulf cryptophytes to obtain new chloroplasts to replace the old ones.¹⁹⁵

Chloroplast DNA

Main article: Chloroplast DNA

Molecular structure

With few exceptions, most chloroplasts have their entire chloroplast genome combined into a single large circular DNA molecule,²⁰² typically 120,000–170,000 base pairs long²⁰³ ²⁰⁴ ²⁰⁵ ²⁰⁶ and a mass of about 80–130 million daltons.²⁰⁷ While chloroplast genomes can almost always be assembled into a circular map, the physical DNA molecules inside cells take on a variety of linear and branching forms.²⁰⁸ ²⁰⁹ New chloroplasts may contain up to 100 copies of their genome,²¹⁰ though the number of copies decreases to about 15–20 as the chloroplasts age.²¹¹

Chloroplast DNA is usually condensed into nucleoids, which can contain multiple copies of the chloroplast genome. Many nucleoids can be found in each chloroplast.²¹² In primitive red algae, the chloroplast DNA nucleoids are clustered in the center of the chloroplast, while in green plants and green algae, the nucleoids are dispersed throughout the stroma.²¹³ Chloroplast DNA is not associated with true histones, proteins that are used to pack DNA molecules tightly in eukaryote nuclei.²¹⁴ Though in red algae, similar proteins tightly pack each chloroplast DNA ring in a nucleoid.²¹⁵

Many chloroplast genomes contain two inverted repeats, which separate a long single copy section (LSC) from a short single copy section (SSC).²¹⁶ A given pair of inverted repeats are rarely identical, but they are always very similar to each other, apparently resulting from concerted evolution.²¹⁷ The inverted repeats vary wildly in length, ranging from 4,000 to 25,000 base pairs long each and containing as few as four or as many as over 150 genes.²¹⁸ The inverted repeat regions are highly conserved in land plants, and accumulate few mutations.²¹⁹ ²²⁰

Similar inverted repeats exist in the genomes of cyanobacteria and the other two chloroplast lineages (glaucophyta and rhodophyceae), suggesting that they predate the chloroplast.²²¹ Some chloroplast genomes have since lost²²² ²²³ or flipped the inverted repeats (making them direct repeats).²²⁴ It is possible that the inverted repeats help stabilize the rest of the chloroplast genome, as chloroplast genomes which have lost some of the inverted repeat segments tend to get rearranged more.²²⁵

DNA repair and replication

In chloroplasts of the moss Physcomitrella patens, the DNA mismatch repair protein Msh1 interacts with the recombinational repair proteins RecA and RecG to maintain chloroplast genome stability.²²⁶ In chloroplasts of the plant Arabidopsis thaliana the RecA protein maintains the integrity of the chloroplast's DNA by a process that likely involves the recombinational repair of DNA damage.²²⁷

The mechanism for chloroplast DNA (cpDNA) replication has not been conclusively determined, but two main models have been proposed. Scientists have attempted to observe chloroplast replication via electron microscopy since the 1970s.²²⁸ ²²⁹ The results of the microscopy experiments led to the idea that chloroplast DNA replicates using a double displacement loop (D-loop). As the D-loop moves through the circular DNA, it adopts a theta intermediary form, also known as a Cairns replication intermediate, and completes replication with a rolling circle mechanism.²³⁰ ²³¹ Transcription starts at specific points of origin. Multiple replication forks open up, allowing replication machinery to transcribe the DNA. As replication continues, the forks grow and eventually converge. The new cpDNA structures separate, creating daughter cpDNA chromosomes.

In addition to the early microscopy experiments, this model is also supported by the amounts of deamination seen in cpDNA.²³² Deamination occurs when an amino group is lost and is a mutation that often results in base changes. When adenine is deaminated, it becomes hypoxanthine. Hypoxanthine can bind to cytosine, and when the XC base pair is replicated, it becomes a GC (thus, an A → G base change).²³³

In cpDNA, there are several A → G deamination gradients. DNA becomes susceptible to deamination events when it is single stranded. When replication forks form, the strand not being copied is single stranded, and thus at risk for A → G deamination. Therefore, gradients in deamination indicate that replication forks were most likely present and the direction that they initially opened (the highest gradient is most likely nearest the start site because it was single stranded for the longest amount of time).²³⁴ This mechanism is still the leading theory today; however, a second theory suggests that most cpDNA is actually linear and replicates through homologous recombination. It further contends that only a minority of the genetic material is kept in circular chromosomes while the rest is in branched, linear, or other complex structures.²³⁵ ²³⁶

One of competing model for cpDNA replication asserts that most cpDNA is linear and participates in homologous recombination and replication structures similar to the linear and circular DNA structures of bacteriophage T4.²³⁷ ²³⁸ It has been established that some plants have linear cpDNA, such as maize, and that more species still contain complex structures that scientists do not yet understand.²³⁹ When the original experiments on cpDNA were performed, scientists did notice linear structures; however, they attributed these linear forms to broken circles.²⁴⁰ If the branched and complex structures seen in cpDNA experiments are real and not artifacts of concatenated circular DNA or broken circles, then a D-loop mechanism of replication is insufficient to explain how those structures would replicate.²⁴¹ At the same time, homologous recombination does not expand the multiple A --> G gradients seen in plastomes.²⁴² Because of the failure to explain the deamination gradient as well as the numerous plant species that have been shown to have circular cpDNA, the predominant theory continues to hold that most cpDNA is circular and most likely replicates via a D loop mechanism.

Gene content and protein synthesis

The ancestral cyanobacteria that led to chloroplasts probably had a genome that contained over 3000 genes, but only approximately 100 genes remain in contemporary chloroplast genomes.²⁴³ ²⁴⁴ ²⁴⁵ These genes code for a variety of things, mostly to do with the protein pipeline and photosynthesis. As in prokaryotes, genes in chloroplast DNA are organized into operons.²⁴⁶ Unlike prokaryotic DNA molecules, chloroplast DNA molecules contain introns (plant mitochondrial DNAs do too, but not human mtDNAs).²⁴⁷

Among land plants, the contents of the chloroplast genome are fairly similar.²⁴⁸

Chloroplast genome reduction and gene transfer

Over time, many parts of the chloroplast genome were transferred to the nuclear genome of the host,²⁴⁹ ²⁵⁰ ²⁵¹ a process called endosymbiotic gene transfer. As a result, the chloroplast genome is heavily reduced compared to that of free-living cyanobacteria. Chloroplasts may contain 60–100 genes whereas cyanobacteria often have more than 1500 genes in their genome.²⁵² Recently, a plastid without a genome was found, demonstrating chloroplasts can lose their genome during endosymbiotic the gene transfer process.²⁵³

Endosymbiotic gene transfer is how we know about the lost chloroplasts in many CASH lineages. Even if a chloroplast is eventually lost, the genes it donated to the former host's nucleus persist, providing evidence for the lost chloroplast's existence. For example, while diatoms (a heterokontophyte) now have a red algal derived chloroplast, the presence of many green algal genes in the diatom nucleus provide evidence that the diatom ancestor had a green algal derived chloroplast at some point, which was subsequently replaced by the red chloroplast.²⁵⁴

In land plants, some 11–14% of the DNA in their nuclei can be traced back to the chloroplast,²⁵⁵ up to 18% in Arabidopsis, corresponding to about 4,500 protein-coding genes.²⁵⁶ There have been a few recent transfers of genes from the chloroplast DNA to the nuclear genome in land plants.²⁵⁷

Of the approximately 3000 proteins found in chloroplasts, some 95% of them are encoded by nuclear genes. Many of the chloroplast's protein complexes consist of subunits from both the chloroplast genome and the host's nuclear genome. As a result, protein synthesis must be coordinated between the chloroplast and the nucleus. The chloroplast is mostly under nuclear control, though chloroplasts can also give out signals regulating gene expression in the nucleus, called retrograde signaling.²⁵⁸ Recent research indicates that parts of the retrograde signaling network once considered characteristic for land plants emerged already in an algal progenitor,²⁵⁹ ²⁶⁰ ²⁶¹ integrating into co-expressed cohorts of genes in the closest algal relatives of land plants.²⁶²

Protein synthesis

Protein targeting and import

Transport proteins and membrane translocons

After a chloroplast polypeptide is synthesized on a ribosome in the cytosol, an enzyme specific to chloroplast proteins²⁷² phosphorylates, or adds a phosphate group to many (but not all) of them in their transit sequences.²⁷³ Phosphorylation helps many proteins bind the polypeptide, keeping it from folding prematurely.²⁷⁴ This is important because it prevents chloroplast proteins from assuming their active form and carrying out their chloroplast functions in the wrong place—the cytosol.²⁷⁵ ²⁷⁶ At the same time, they have to keep just enough shape so that they can be recognized by the chloroplast.²⁷⁷ These proteins also help the polypeptide get imported into the chloroplast.²⁷⁸

From here, chloroplast proteins bound for the stroma must pass through two protein complexes—the TOC complex, or translocon on the outer chloroplast membrane, and the TIC translocon, or translocon on the inner chloroplast membrane translocon.²⁷⁹ Chloroplast polypeptide chains probably often travel through the two complexes at the same time, but the TIC complex can also retrieve preproteins lost in the intermembrane space.²⁸⁰

Structure

In land plants, chloroplasts are generally lens-shaped, 3–10 μm in diameter and 1–3 μm thick.²⁸¹ ²⁸² Corn seedling chloroplasts are ≈20 μm3 in volume.²⁸³ Greater diversity in chloroplast shapes exists among the algae, which often contain a single chloroplast²⁸⁴ that can be shaped like a net (e.g., Oedogonium),²⁸⁵ a cup (e.g., Chlamydomonas),²⁸⁶ a ribbon-like spiral around the edges of the cell (e.g., Spirogyra),²⁸⁷ or slightly twisted bands at the cell edges (e.g., Sirogonium).²⁸⁸ Some algae have two chloroplasts in each cell; they are star-shaped in Zygnema,²⁸⁹ or may follow the shape of half the cell in order Desmidiales.²⁹⁰ In some algae, the chloroplast takes up most of the cell, with pockets for the nucleus and other organelles,²⁹¹ for example, some species of Chlorella have a cup-shaped chloroplast that occupies much of the cell.²⁹²

All chloroplasts have at least three membrane systems—the outer chloroplast membrane, the inner chloroplast membrane, and the thylakoid system. The two innermost lipid-bilayer membranes ²⁹³ that surround all chloroplasts correspond to the outer and inner membranes of the ancestral cyanobacterium's gram negative cell wall,²⁹⁴ ²⁹⁵ ²⁹⁶ and not the phagosomal membrane from the host, which was probably lost.²⁹⁷ Chloroplasts that are the product of secondary endosymbiosis may have additional membranes surrounding these three.²⁹⁸ Inside the outer and inner chloroplast membranes is the chloroplast stroma, a semi-gel-like fluid²⁹⁹ that makes up much of a chloroplast's volume, and in which the thylakoid system floats.

Outer chloroplast membrane

Main article: Chloroplast membrane

The outer chloroplast membrane is a semi-porous membrane that small molecules and ions can easily diffuse across.³⁰⁴ However, it is not permeable to larger proteins, so chloroplast polypeptides being synthesized in the cell cytoplasm must be transported across the outer chloroplast membrane by the TOC complex, or translocon on the outer chloroplast membrane.³⁰⁵

The chloroplast membranes sometimes protrude out into the cytoplasm, forming a stromule, or stroma-containing tubule. Stromules are very rare in chloroplasts, and are much more common in other plastids like chromoplasts and amyloplasts in petals and roots, respectively.³⁰⁶ ³⁰⁷ They may exist to increase the chloroplast's surface area for cross-membrane transport, because they are often branched and tangled with the endoplasmic reticulum.³⁰⁸ When they were first observed in 1962, some plant biologists dismissed the structures as artifactual, claiming that stromules were just oddly shaped chloroplasts with constricted regions or dividing chloroplasts.³⁰⁹ However, there is a growing body of evidence that stromules are functional, integral features of plant cell plastids, not merely artifacts.³¹⁰

Intermembrane space and peptidoglycan wall

Usually, a thin intermembrane space about 10–20 nanometers thick exists between the outer and inner chloroplast membranes.³¹¹

Glaucophyte algal chloroplasts have a peptidoglycan layer between the chloroplast membranes. It corresponds to the peptidoglycan cell wall of their cyanobacterial ancestors, which is located between their two cell membranes. These chloroplasts are called muroplasts (from Latin "mura", meaning "wall"). Other chloroplasts were assumed to have lost the cyanobacterial wall, leaving an intermembrane space between the two chloroplast envelope membranes,³¹² but has since been found also in moss, lycophytes and ferns.³¹³

Inner chloroplast membrane

Main article: Chloroplast membrane

The inner chloroplast membrane borders the stroma and regulates passage of materials in and out of the chloroplast. After passing through the TOC complex in the outer chloroplast membrane, polypeptides must pass through the TIC complex (translocon on the inner chloroplast membrane) which is located in the inner chloroplast membrane.³¹⁴

In addition to regulating the passage of materials, the inner chloroplast membrane is where fatty acids, lipids, and carotenoids are synthesized.³¹⁵

Peripheral reticulum

Some chloroplasts contain a structure called the chloroplast peripheral reticulum.³¹⁶ It is often found in the chloroplasts of C4 plants, though it has also been found in some C3 angiosperms,³¹⁷ and even some gymnosperms.³¹⁸ The chloroplast peripheral reticulum consists of a maze of membranous tubes and vesicles continuous with the inner chloroplast membrane that extends into the internal stromal fluid of the chloroplast. Its purpose is thought to be to increase the chloroplast's surface area for cross-membrane transport between its stroma and the cell cytoplasm. The small vesicles sometimes observed may serve as transport vesicles to shuttle stuff between the thylakoids and intermembrane space.³¹⁹

Stroma

Main article: Stroma

The protein-rich,³²⁰ alkaline,³²¹ aqueous fluid within the inner chloroplast membrane and outside of the thylakoid space is called the stroma,³²² which corresponds to the cytosol of the original cyanobacterium. Nucleoids of chloroplast DNA, chloroplast ribosomes, the thylakoid system with plastoglobuli, starch granules, and many proteins can be found floating around in it. The Calvin cycle, which fixes CO2 into G3P takes place in the stroma.

Chloroplast ribosomes

Chloroplasts have their own ribosomes, which they use to synthesize a small fraction of their proteins. Chloroplast ribosomes are about two-thirds the size of cytoplasmic ribosomes (around 17 nm vs 25 nm).³²³ They take mRNAs transcribed from the chloroplast DNA and translate them into protein. While similar to bacterial ribosomes,³²⁴ chloroplast translation is more complex than in bacteria, so chloroplast ribosomes include some chloroplast-unique features.³²⁵ ³²⁶

Small subunit ribosomal RNAs in several Chlorophyta and euglenid chloroplasts lack motifs for Shine-Dalgarno sequence recognition,³²⁷ which is considered essential for translation initiation in most chloroplasts and prokaryotes.³²⁸ ³²⁹ Such loss is also rarely observed in other plastids and prokaryotes.³³⁰ ³³¹ An additional 4.5S rRNA with homology to the 3' tail of 23S is found in "higher" plants.³³²

Plastoglobuli

Plastoglobuli (singular plastoglobulus, sometimes spelled plastoglobule(s)), are spherical bubbles of lipids and proteins ³³³ about 45–60 nanometers across.³³⁴ They are surrounded by a lipid monolayer.³³⁵ Plastoglobuli are found in all chloroplasts,³³⁶ but become more common when the chloroplast is under oxidative stress,³³⁷ or when it ages and transitions into a gerontoplast.³³⁸ Plastoglobuli also exhibit a greater size variation under these conditions.³³⁹ They are also common in etioplasts, but decrease in number as the etioplasts mature into chloroplasts.³⁴⁰

Plastoglobuli contain both structural proteins and enzymes involved in lipid synthesis and metabolism. They contain many types of lipids including plastoquinone, vitamin E, carotenoids and chlorophylls.³⁴¹

Plastoglobuli were once thought to be free-floating in the stroma, but it is now thought that they are permanently attached either to a thylakoid or to another plastoglobulus attached to a thylakoid, a configuration that allows a plastoglobulus to exchange its contents with the thylakoid network.³⁴² In normal green chloroplasts, the vast majority of plastoglobuli occur singularly, attached directly to their parent thylakoid. In old or stressed chloroplasts, plastoglobuli tend to occur in linked groups or chains, still always anchored to a thylakoid.³⁴³

Plastoglobuli form when a bubble appears between the layers of the lipid bilayer of the thylakoid membrane, or bud from existing plastoglobuli—though they never detach and float off into the stroma.³⁴⁴ Practically all plastoglobuli form on or near the highly curved edges of the thylakoid disks or sheets. They are also more common on stromal thylakoids than on granal ones.³⁴⁵

Starch granules

Starch granules are very common in chloroplasts, typically taking up 15% of the organelle's volume,³⁴⁶ though in some other plastids like amyloplasts, they can be big enough to distort the shape of the organelle.³⁴⁷ Starch granules are simply accumulations of starch in the stroma, and are not bounded by a membrane.³⁴⁸

Starch granules appear and grow throughout the day, as the chloroplast synthesizes sugars, and are consumed at night to fuel respiration and continue sugar export into the phloem,³⁴⁹ though in mature chloroplasts, it is rare for a starch granule to be completely consumed or for a new granule to accumulate.³⁵⁰

Starch granules vary in composition and location across different chloroplast lineages. In red algae, starch granules are found in the cytoplasm rather than in the chloroplast.³⁵¹ In C4 plants, mesophyll chloroplasts, which do not synthesize sugars, lack starch granules.³⁵²

RuBisCO

Main article: RuBisCO

The chloroplast stroma contains many proteins, though the most common and important is RuBisCO, which is probably also the most abundant protein on the planet.³⁵³ RuBisCO is the enzyme that fixes CO2 into sugar molecules. In C3 plants, RuBisCO is abundant in all chloroplasts, though in C4 plants, it is confined to the bundle sheath chloroplasts, where the Calvin cycle is carried out in C4 plants.³⁵⁴

Pyrenoids

Main article: Pyrenoid

The chloroplasts of some hornworts ³⁵⁵ and algae contain structures called pyrenoids. They are not found in higher plants.³⁵⁶ Pyrenoids are roughly spherical and highly refractive bodies which are a site of starch accumulation in plants that contain them. They consist of a matrix opaque to electrons, surrounded by two hemispherical starch plates. The starch is accumulated as the pyrenoids mature.³⁵⁷ In algae with carbon concentrating mechanisms, the enzyme RuBisCO is found in the pyrenoids. Starch can also accumulate around the pyrenoids when CO2 is scarce.³⁵⁸ Pyrenoids can divide to form new pyrenoids, or be produced "de novo".³⁵⁹ ³⁶⁰

Thylakoid system

Main article: Thylakoid

Thylakoids (sometimes spelled thylakoïds),³⁶¹ are small interconnected sacks which contain the membranes that the light reactions of photosynthesis take place on. The word thylakoid comes from the Greek word thylakos which means "sack".³⁶²

Suspended within the chloroplast stroma is the thylakoid system, a highly dynamic collection of membranous sacks called thylakoids where chlorophyll is found and the light reactions of photosynthesis happen.³⁶³ In most vascular plant chloroplasts, the thylakoids are arranged in stacks called grana,³⁶⁴ though in certain C4 plant chloroplasts³⁶⁵ and some algal chloroplasts, the thylakoids are free floating.³⁶⁶

Thylakoid structure

Using a light microscope, it is just barely possible to see tiny green granules—which were named grana.³⁶⁷ With electron microscopy, it became possible to see the thylakoid system in more detail, revealing it to consist of stacks of flat thylakoids which made up the grana, and long interconnecting stromal thylakoids which linked different grana.³⁶⁸ In the transmission electron microscope, thylakoid membranes appear as alternating light-and-dark bands, 8.5 nanometers thick.³⁶⁹

The three-dimensional structure of the thylakoid membrane system has been disputed. Many models have been proposed, the most prevalent being the helical model, in which granum stacks of thylakoids are wrapped by helical stromal thylakoids.³⁷⁰ Another model known as the 'bifurcation model', which was based on the first electron tomography study of plant thylakoid membranes, depicts the stromal membranes as wide lamellar sheets perpendicular to the grana columns which bifurcates into multiple parallel discs forming the granum-stroma assembly.³⁷¹ The helical model was supported by several additional works,³⁷² ³⁷³ but ultimately it was determined in 2019 that features from both the helical and bifurcation models are consolidated by newly discovered left-handed helical membrane junctions.³⁷⁴ Likely for ease, the thylakoid system is still commonly depicted by older "hub and spoke" models where the grana are connected to each other by tubes of stromal thylakoids.³⁷⁵

Grana consist of a stacks of flattened circular granal thylakoids that resemble pancakes. Each granum can contain anywhere from two to a hundred thylakoids,³⁷⁶ though grana with 10–20 thylakoids are most common.³⁷⁷ Wrapped around the grana are multiple parallel right-handed helical stromal thylakoids, also known as frets or lamellar thylakoids. The helices ascend at an angle of ~20°, connecting to each granal thylakoid at a bridge-like slit junction.³⁷⁸ ³⁷⁹ ³⁸⁰

The stroma lamellae extend as large sheets perpendicular to the grana columns. These sheets are connected to the right-handed helices either directly or through bifurcations that form left-handed helical membrane surfaces.³⁸¹ The left-handed helical surfaces have a similar tilt angle to the right-handed helices (~20°), but ¼ the pitch. Approximately 4 left-handed helical junctions are present per granum, resulting in a pitch-balanced array of right- and left-handed helical membrane surfaces of different radii and pitch that consolidate the network with minimal surface and bending energies.³⁸² While different parts of the thylakoid system contain different membrane proteins, the thylakoid membranes are continuous and the thylakoid space they enclose form a single continuous labyrinth.³⁸³

Thylakoid composition

Embedded in the thylakoid membranes are important protein complexes which carry out the light reactions of photosynthesis. Photosystem II and photosystem I contain light-harvesting complexes with chlorophyll and carotenoids that absorb light energy and use it to energize electrons. Molecules in the thylakoid membrane use the energized electrons to pump hydrogen ions into the thylakoid space, decreasing the pH and turning it acidic. ATP synthase is a large protein complex that harnesses the concentration gradient of the hydrogen ions in the thylakoid space to generate ATP energy as the hydrogen ions flow back out into the stroma—much like a dam turbine.³⁸⁴

There are two types of thylakoids—granal thylakoids, which are arranged in grana, and stromal thylakoids, which are in contact with the stroma. Granal thylakoids are pancake-shaped circular disks about 300–600 nanometers in diameter. Stromal thylakoids are helicoid sheets that spiral around grana.³⁸⁵ The flat tops and bottoms of granal thylakoids contain only the relatively flat photosystem II protein complex. This allows them to stack tightly, forming grana with many layers of tightly appressed membrane, called granal membrane, increasing stability and surface area for light capture.³⁸⁶

In contrast, photosystem I and ATP synthase are large protein complexes which jut out into the stroma. They can't fit in the appressed granal membranes, and so are found in the stromal thylakoid membrane—the edges of the granal thylakoid disks and the stromal thylakoids. These large protein complexes may act as spacers between the sheets of stromal thylakoids.³⁸⁷

The number of thylakoids and the total thylakoid area of a chloroplast is influenced by light exposure. Shaded chloroplasts contain larger and more grana with more thylakoid membrane area than chloroplasts exposed to bright light, which have smaller and fewer grana and less thylakoid area. Thylakoid extent can change within minutes of light exposure or removal.³⁸⁸

Pigments and chloroplast colors

Inside the photosystems embedded in chloroplast thylakoid membranes are various photosynthetic pigments, which absorb and transfer light energy. The types of pigments found are different in various groups of chloroplasts, and are responsible for a wide variety of chloroplast colorations. Other plastid types, such as the leucoplast and the chromoplast, contain little chlorophyll and do not carry out photosynthesis.

Paper chromatography of some spinach leaf extract shows the various pigments present in their chloroplasts. Xanthophylls Chlorophyll a Chlorophyll b

Chlorophylls

Chlorophyll a is found in all chloroplasts, as well as their cyanobacterial ancestors. Chlorophyll a is a blue-green pigment³⁸⁹ partially responsible for giving most cyanobacteria and chloroplasts their color. Other forms of chlorophyll exist, such as the accessory pigments chlorophyll b, chlorophyll c, chlorophyll d,³⁹⁰ and chlorophyll f.

Chlorophyll b is an olive green pigment found only in the chloroplasts of plants, green algae, any secondary chloroplasts obtained through the secondary endosymbiosis of a green alga, and a few cyanobacteria.³⁹¹ It is the chlorophylls a and b together that make most plant and green algal chloroplasts green.³⁹²

Chlorophyll c is mainly found in secondary endosymbiotic chloroplasts that originated from a red alga, although it is not found in chloroplasts of red algae themselves. Chlorophyll c is also found in some green algae and cyanobacteria.³⁹³

Chlorophylls d and f are pigments found only in some cyanobacteria.³⁹⁴ ³⁹⁵

Carotenoids

In addition to chlorophylls, another group of yellow–orange ³⁹⁶ pigments called carotenoids are also found in the photosystems. There are about thirty photosynthetic carotenoids.³⁹⁷ They help transfer and dissipate excess energy,³⁹⁸ and their bright colors sometimes override the chlorophyll green, like during the fall, when the leaves of some land plants change color.³⁹⁹ β-carotene is a bright red-orange carotenoid found in nearly all chloroplasts, like chlorophyll a.⁴⁰⁰ Xanthophylls, especially the orange-red zeaxanthin, are also common.⁴⁰¹ Many other forms of carotenoids exist that are only found in certain groups of chloroplasts.⁴⁰²

Phycobilins

Phycobilins are a third group of pigments found in cyanobacteria, and glaucophyte, red algal, and cryptophyte chloroplasts.⁴⁰³ ⁴⁰⁴ Phycobilins come in all colors, though phycoerytherin is one of the pigments that makes many red algae red.⁴⁰⁵ Phycobilins often organize into relatively large protein complexes about 40 nanometers across called phycobilisomes.⁴⁰⁶ Like photosystem I and ATP synthase, phycobilisomes jut into the stroma, preventing thylakoid stacking in red algal chloroplasts.⁴⁰⁷ Cryptophyte chloroplasts and some cyanobacteria don't have their phycobilin pigments organized into phycobilisomes, and keep them in their thylakoid space instead.⁴⁰⁸

Photosynthetic pigments. Presence of pigments across chloroplast groups and cyanobacteria. Colored cells represent pigment presence. Chl = chlorophyll⁴⁰⁹ ⁴¹⁰ ⁴¹¹
	Chl a	Chl b	Chl c	Chl d and f	Xanthophylls	α-carotene	β-carotene	Phycobilins
Land plants
Green algae
Euglenophytes and Chlorarachniophytes
Euglenophytes and Chlorarachniophytes
Multicellular red algae
Unicellular red algae
Haptophytes and Dinophytes
Haptophytes and Dinophytes
Cryptophytes
Glaucophytes
Cyanobacteria

Specialized chloroplasts in C4 plants

See also: Photosynthesis and C4 photosynthesis

To fix carbon dioxide into sugar molecules in the process of photosynthesis, chloroplasts use an enzyme called RuBisCO. RuBisCO has trouble distinguishing between carbon dioxide and oxygen, so at high oxygen concentrations, RuBisCO starts accidentally adding oxygen to sugar precursors. This has the result of ATP energy being wasted and CO2 being released, all with no sugar being produced. This is a big problem, since O2 is produced by the initial light reactions of photosynthesis, causing issues down the line in the Calvin cycle which uses RuBisCO.⁴¹²

C4 plants evolved a way to solve this—by spatially separating the light reactions and the Calvin cycle. The light reactions, which store light energy in ATP and NADPH, are done in the mesophyll cells of a C4 leaf. The Calvin cycle, which uses the stored energy to make sugar using RuBisCO, is done in the bundle sheath cells, a layer of cells surrounding a vein in a leaf.⁴¹³

As a result, chloroplasts in C4 mesophyll cells and bundle sheath cells are specialized for each stage of photosynthesis. In mesophyll cells, chloroplasts are specialized for the light reactions, so they lack RuBisCO, and have normal grana and thylakoids,⁴¹⁴ which they use to make ATP and NADPH, as well as oxygen. They store CO2 in a four-carbon compound, which is why the process is called C4 photosynthesis. The four-carbon compound is then transported to the bundle sheath chloroplasts, where it drops off CO2 and returns to the mesophyll. Bundle sheath chloroplasts do not carry out the light reactions, preventing oxygen from building up in them and disrupting RuBisCO activity.⁴¹⁵ Because of this, they lack thylakoids organized into grana stacks—though bundle sheath chloroplasts still have free-floating thylakoids in the stroma where they still carry out cyclic electron flow, a light-driven method of synthesizing ATP to power the Calvin cycle without generating oxygen. They lack photosystem II, and only have photosystem I—the only protein complex needed for cyclic electron flow.⁴¹⁶ ⁴¹⁷ Because the job of bundle sheath chloroplasts is to carry out the Calvin cycle and make sugar, they often contain large starch grains.⁴¹⁸

Both types of chloroplast contain large amounts of chloroplast peripheral reticulum,⁴¹⁹ which they use to get more surface area to transport stuff in and out of them.⁴²⁰ ⁴²¹ Mesophyll chloroplasts have a little more peripheral reticulum than bundle sheath chloroplasts.⁴²²

Function and chemistry

Guard cell chloroplasts

Unlike most epidermal cells, the guard cells of plant stomata contain relatively well-developed chloroplasts.⁴²³ However, exactly what they do is controversial.⁴²⁴

Plant innate immunity

Plants lack specialized immune cells—all plant cells participate in the plant immune response. Chloroplasts, along with the nucleus, cell membrane, and endoplasmic reticulum,⁴²⁵ are key players in pathogen defense. Due to its role in a plant cell's immune response, pathogens frequently target the chloroplast.⁴²⁶

Plants have two main immune responses—the hypersensitive response, in which infected cells seal themselves off and undergo programmed cell death, and systemic acquired resistance, where infected cells release signals warning the rest of the plant of a pathogen's presence. Chloroplasts stimulate both responses by purposely damaging their photosynthetic system, producing reactive oxygen species. High levels of reactive oxygen species will cause the hypersensitive response. The reactive oxygen species also directly kill any pathogens within the cell. Lower levels of reactive oxygen species initiate systemic acquired resistance, triggering defense-molecule production in the rest of the plant.⁴²⁷

In some plants, chloroplasts are known to move closer to the infection site and the nucleus during an infection.⁴²⁸

Chloroplasts can serve as cellular sensors. After detecting stress in a cell, which might be due to a pathogen, chloroplasts begin producing molecules like salicylic acid, jasmonic acid, nitric oxide and reactive oxygen species which can serve as defense-signals. As cellular signals, reactive oxygen species are unstable molecules, so they probably don't leave the chloroplast, but instead pass on their signal to an unknown second messenger molecule. All these molecules initiate retrograde signaling—signals from the chloroplast that regulate gene expression in the nucleus.⁴²⁹

In addition to defense signaling, chloroplasts, with the help of the peroxisomes,⁴³⁰ help synthesize an important defense molecule, jasmonate. Chloroplasts synthesize all the fatty acids in a plant cell⁴³¹ ⁴³²—linoleic acid, a fatty acid, is a precursor to jasmonate.⁴³³

Photosynthesis

Main article: Photosynthesis

One of the main functions of the chloroplast is its role in photosynthesis, the process by which light is transformed into chemical energy, to subsequently produce food in the form of sugars. Water (H2O) and carbon dioxide (CO2) are used in photosynthesis, and sugar and oxygen (O2) are made, using light energy. Photosynthesis is divided into two stages—the light reactions, where water is split to produce oxygen, and the dark reactions, or Calvin cycle, which builds sugar molecules from carbon dioxide. The two phases are linked by the energy carriers adenosine triphosphate (ATP) and nicotinamide adenine dinucleotide phosphate (NADP+).⁴³⁴ ⁴³⁵

Light reactions

Main article: Light reactions

The light reactions take place on the thylakoid membranes. They take light energy and store it in NADPH, a form of NADP+, and ATP to fuel the dark reactions.

Energy carriers

Main articles: Adenosine triphosphate and NADPH

ATP is the phosphorylated version of adenosine diphosphate (ADP), which stores energy in a cell and powers most cellular activities. ATP is the energized form, while ADP is the (partially) depleted form. NADP+ is an electron carrier which ferries high energy electrons. In the light reactions, it gets reduced, meaning it picks up electrons, becoming NADPH.

Photophosphorylation

Main article: Photophosphorylation

Like mitochondria, chloroplasts use the potential energy stored in an H+, or hydrogen ion, gradient to generate ATP energy. The two photosystems capture light energy to energize electrons taken from water, and release them down an electron transport chain. The molecules between the photosystems harness the electrons' energy to pump hydrogen ions into the thylakoid space, creating a concentration gradient, with more hydrogen ions (up to a thousand times as many)⁴³⁶ inside the thylakoid system than in the stroma. The hydrogen ions in the thylakoid space then diffuse back down their concentration gradient, flowing back out into the stroma through ATP synthase. ATP synthase uses the energy from the flowing hydrogen ions to phosphorylate adenosine diphosphate into adenosine triphosphate, or ATP.⁴³⁷ ⁴³⁸ Because chloroplast ATP synthase projects out into the stroma, the ATP is synthesized there, in position to be used in the dark reactions.⁴³⁹

NADP+ reduction

Cyclic photophosphorylation

Main article: Cyclic photophosphorylation

While photosystem II photolyzes water to obtain and energize new electrons, photosystem I simply reenergizes depleted electrons at the end of an electron transport chain. Normally, the reenergized electrons are taken by NADP+, though sometimes they can flow back down more H+-pumping electron transport chains to transport more hydrogen ions into the thylakoid space to generate more ATP. This is termed cyclic photophosphorylation because the electrons are recycled. Cyclic photophosphorylation is common in C4 plants, which need more ATP than NADPH.⁴⁴³

Dark reactions

Main article: Dark reactions

The Calvin cycle, also known as the dark reactions, is a series of biochemical reactions that fixes CO2 into G3P sugar molecules and uses the energy and electrons from the ATP and NADPH made in the light reactions. The Calvin cycle takes place in the stroma of the chloroplast.⁴⁴⁴

While named "the dark reactions", in most plants, they take place in the light, since the dark reactions are dependent on the products of the light reactions.⁴⁴⁵

Carbon fixation and G3P synthesis

The Calvin cycle starts by using the enzyme RuBisCO to fix CO2 into five-carbon Ribulose bisphosphate (RuBP) molecules. The result is unstable six-carbon molecules that immediately break down into three-carbon molecules called 3-phosphoglyceric acid, or 3-PGA. The ATP and NADPH made in the light reactions is used to convert the 3-PGA into glyceraldehyde-3-phosphate, or G3P sugar molecules. Most of the G3P molecules are recycled back into RuBP using energy from more ATP, but one out of every six produced leaves the cycle—the end product of the dark reactions.⁴⁴⁶

Sugars and starches

Glyceraldehyde-3-phosphate can double up to form larger sugar molecules like glucose and fructose. These molecules are processed, and from them, the still larger sucrose, a disaccharide commonly known as table sugar, is made, though this process takes place outside of the chloroplast, in the cytoplasm.⁴⁴⁷

Alternatively, glucose monomers in the chloroplast can be linked together to make starch, which accumulates into the starch grains found in the chloroplast.⁴⁴⁸ Under conditions such as high atmospheric CO2 concentrations, these starch grains may grow very large, distorting the grana and thylakoids. The starch granules displace the thylakoids, but leave them intact.⁴⁴⁹ Waterlogged roots can also cause starch buildup in the chloroplasts, possibly due to less sucrose being exported out of the chloroplast (or more accurately, the plant cell). This depletes a plant's free phosphate supply, which indirectly stimulates chloroplast starch synthesis.⁴⁵⁰ While linked to low photosynthesis rates, the starch grains themselves may not necessarily interfere significantly with the efficiency of photosynthesis,⁴⁵¹ and might simply be a side effect of another photosynthesis-depressing factor.⁴⁵²

Photorespiration

Photorespiration can occur when the oxygen concentration is too high. RuBisCO cannot distinguish between oxygen and carbon dioxide very well, so it can accidentally add O2 instead of CO2 to RuBP. This process reduces the efficiency of photosynthesis—it consumes ATP and oxygen, releases CO2, and produces no sugar. It can waste up to half the carbon fixed by the Calvin cycle.⁴⁵³ Several mechanisms have evolved in different lineages that raise the carbon dioxide concentration relative to oxygen within the chloroplast, increasing the efficiency of photosynthesis. These mechanisms are called carbon dioxide concentrating mechanisms, or CCMs. These include Crassulacean acid metabolism, C4 carbon fixation,⁴⁵⁴ and pyrenoids. Chloroplasts in C4 plants are notable as they exhibit a distinct chloroplast dimorphism.

pH

Because of the H+ gradient across the thylakoid membrane, the interior of the thylakoid is acidic, with a pH around 4,⁴⁵⁵ while the stroma is slightly basic, with a pH of around 8.⁴⁵⁶ The optimal stroma pH for the Calvin cycle is 8.1, with the reaction nearly stopping when the pH falls below 7.3.⁴⁵⁷

CO2 in water can form carbonic acid, which can disturb the pH of isolated chloroplasts, interfering with photosynthesis, even though CO2 is used in photosynthesis. However, chloroplasts in living plant cells are not affected by this as much.⁴⁵⁸

Chloroplasts can pump K+ and H+ ions in and out of themselves using a poorly understood light-driven transport system.⁴⁵⁹

In the presence of light, the pH of the thylakoid lumen can drop up to 1.5 pH units, while the pH of the stroma can rise by nearly one pH unit.⁴⁶⁰

Amino acid synthesis

Chloroplasts alone make almost all of a plant cell's amino acids in their stroma ⁴⁶¹ except the sulfur-containing ones like cysteine and methionine.⁴⁶² ⁴⁶³ Cysteine is made in the chloroplast (the proplastid too) but it is also synthesized in the cytosol and mitochondria, probably because it has trouble crossing membranes to get to where it is needed.⁴⁶⁴ The chloroplast is known to make the precursors to methionine but it is unclear whether the organelle carries out the last leg of the pathway or if it happens in the cytosol.⁴⁶⁵

Other nitrogen compounds

Chloroplasts make all of a cell's purines and pyrimidines—the nitrogenous bases found in DNA and RNA.⁴⁶⁶ They also convert nitrite (NO2−) into ammonia (NH3) which supplies the plant with nitrogen to make its amino acids and nucleotides.⁴⁶⁷

Other chemical products

The plastid is the site of diverse and complex lipid synthesis in plants.⁴⁶⁸ ⁴⁶⁹ The carbon used to form the majority of the lipid is from acetyl-CoA, which is the decarboxylation product of pyruvate.⁴⁷⁰ Pyruvate may enter the plastid from the cytosol by passive diffusion through the membrane after production in glycolysis.⁴⁷¹ Pyruvate is also made in the plastid from phosphoenolpyruvate, a metabolite made in the cytosol from pyruvate or PGA.⁴⁷² Acetate in the cytosol is unavailable for lipid biosynthesis in the plastid.⁴⁷³ The typical length of fatty acids produced in the plastid are 16 or 18 carbons, with 0-3 cis double bonds.⁴⁷⁴

The biosynthesis of fatty acids from acetyl-CoA primarily requires two enzymes. Acetyl-CoA carboxylase creates malonyl-CoA, used in both the first step and the extension steps of synthesis. Fatty acid synthase (FAS) is a large complex of enzymes and cofactors including acyl carrier protein (ACP) which holds the acyl chain as it is synthesized. The initiation of synthesis begins with the condensation of malonyl-ACP with acetyl-CoA to produce ketobutyryl-ACP. 2 reductions involving the use of NADPH and one dehydration creates butyryl-ACP. Extension of the fatty acid comes from repeated cycles of malonyl-ACP condensation, reduction, and dehydration.⁴⁷⁵

Other lipids are derived from the methyl-erythritol phosphate (MEP) pathway and consist of gibberelins, sterols, abscisic acid, phytol, and innumerable secondary metabolites.⁴⁷⁶

Location

Distribution in a plant

Not all cells in a multicellular plant contain chloroplasts. All green parts of a plant contain chloroplasts as the color comes from the chlorophyll.⁴⁷⁷ The plant cells which contain chloroplasts are usually parenchyma cells, though chloroplasts can also be found in collenchyma tissue.⁴⁷⁸ A plant cell which contains chloroplasts is known as a chlorenchyma cell. A typical chlorenchyma cell of a land plant contains about 10 to 100 chloroplasts.

In some plants such as cacti, chloroplasts are found in the stems,⁴⁷⁹ though in most plants, chloroplasts are concentrated in the leaves. One square millimeter of leaf tissue can contain half a million chloroplasts.⁴⁸⁰ Within a leaf, chloroplasts are mainly found in the mesophyll layers of a leaf, and the guard cells of stomata. Palisade mesophyll cells can contain 30–70 chloroplasts per cell, while stomatal guard cells contain only around 8–15 per cell, as well as much less chlorophyll. Chloroplasts can also be found in the bundle sheath cells of a leaf, especially in C4 plants, which carry out the Calvin cycle in their bundle sheath cells. They are often absent from the epidermis of a leaf.⁴⁸¹

Cellular location

Chloroplast movement

Differentiation, replication, and inheritance

Main article: Plastid

Chloroplasts are a special type of a plant cell organelle called a plastid, though the two terms are sometimes used interchangeably. There are many other types of plastids, which carry out various functions. All chloroplasts in a plant are descended from undifferentiated proplastids found in the zygote,⁴⁹⁰ or fertilized egg. Proplastids are commonly found in an adult plant's apical meristems. Chloroplasts do not normally develop from proplastids in root tip meristems ⁴⁹¹—instead, the formation of starch-storing amyloplasts is more common.⁴⁹²

In shoots, proplastids from shoot apical meristems can gradually develop into chloroplasts in photosynthetic leaf tissues as the leaf matures, if exposed to the required light.⁴⁹³ This process involves invaginations of the inner plastid membrane, forming sheets of membrane that project into the internal stroma. These membrane sheets then fold to form thylakoids and grana.⁴⁹⁴

If angiosperm shoots are not exposed to the required light for chloroplast formation, proplastids may develop into an etioplast stage before becoming chloroplasts. An etioplast is a plastid that lacks chlorophyll, and has inner membrane invaginations that form a lattice of tubes in their stroma, called a prolamellar body. While etioplasts lack chlorophyll, they have a yellow chlorophyll precursor stocked.⁴⁹⁵ Within a few minutes of light exposure, the prolamellar body begins to reorganize into stacks of thylakoids, and chlorophyll starts to be produced. This process, where the etioplast becomes a chloroplast, takes several hours.⁴⁹⁶ Gymnosperms do not require light to form chloroplasts.⁴⁹⁷

Light, however, does not guarantee that a proplastid will develop into a chloroplast. Whether a proplastid develops into a chloroplast some other kind of plastid is mostly controlled by the nucleus ⁴⁹⁸ and is largely influenced by the kind of cell it resides in.⁴⁹⁹

Plastid interconversion

Plastid differentiation is not permanent, in fact many interconversions are possible. Chloroplasts may be converted to chromoplasts, which are pigment-filled plastids responsible for the bright colors seen in flowers and ripe fruit. Starch storing amyloplasts can also be converted to chromoplasts, and it is possible for proplastids to develop straight into chromoplasts. Chromoplasts and amyloplasts can also become chloroplasts, like what happens when a carrot or a potato is illuminated. If a plant is injured, or something else causes a plant cell to revert to a meristematic state, chloroplasts and other plastids can turn back into proplastids. Chloroplast, amyloplast, chromoplast, proplastid are not absolute; state—intermediate forms are common.⁵⁰⁰

Division

Most chloroplasts in a photosynthetic cell do not develop directly from proplastids or etioplasts. In fact, a typical shoot meristematic plant cell contains only 7–20 proplastids. These proplastids differentiate into chloroplasts, which divide to create the 30–70 chloroplasts found in a mature photosynthetic plant cell. If the cell divides, chloroplast division provides the additional chloroplasts to partition between the two daughter cells.⁵⁰¹

In single-celled algae, chloroplast division is the only way new chloroplasts are formed. There is no proplastid differentiation—when an algal cell divides, its chloroplast divides along with it, and each daughter cell receives a mature chloroplast.⁵⁰²

Almost all chloroplasts in a cell divide, rather than a small group of rapidly dividing chloroplasts.⁵⁰³ Chloroplasts have no definite S-phase—their DNA replication is not synchronized or limited to that of their host cells.⁵⁰⁴ Much of what we know about chloroplast division comes from studying organisms like Arabidopsis and the red alga Cyanidioschyzon merolæ.⁵⁰⁵

Most chloroplasts in plant cells, and all chloroplasts in algae arise from chloroplast division.⁵⁰⁶ Picture references,⁵⁰⁷ ⁵⁰⁸

The division process starts when the proteins FtsZ1 and FtsZ2 assemble into filaments, and with the help of a protein ARC6, form a structure called a Z-ring within the chloroplast's stroma.⁵⁰⁹ ⁵¹⁰ The Min system manages the placement of the Z-ring, ensuring that the chloroplast is cleaved more or less evenly. The protein MinD prevents FtsZ from linking up and forming filaments. Another protein ARC3 may also be involved, but it is not very well understood. These proteins are active at the poles of the chloroplast, preventing Z-ring formation there, but near the center of the chloroplast, MinE inhibits them, allowing the Z-ring to form.⁵¹¹

Next, the two plastid-dividing rings, or PD rings form. The inner plastid-dividing ring is located in the inner side of the chloroplast's inner membrane, and is formed first.⁵¹² The outer plastid-dividing ring is found wrapped around the outer chloroplast membrane. It consists of filaments about 5 nanometers across,⁵¹³ arranged in rows 6.4 nanometers apart, and shrinks to squeeze the chloroplast. This is when chloroplast constriction begins.⁵¹⁴ In a few species like Cyanidioschyzon merolæ, chloroplasts have a third plastid-dividing ring located in the chloroplast's intermembrane space.⁵¹⁵ ⁵¹⁶

Late into the constriction phase, dynamin proteins assemble around the outer plastid-dividing ring,⁵¹⁷ helping provide force to squeeze the chloroplast.⁵¹⁸ Meanwhile, the Z-ring and the inner plastid-dividing ring break down.⁵¹⁹ During this stage, the many chloroplast DNA plasmids floating around in the stroma are partitioned and distributed to the two forming daughter chloroplasts.⁵²⁰

Later, the dynamins migrate under the outer plastid dividing ring, into direct contact with the chloroplast's outer membrane,⁵²¹ to cleave the chloroplast in two daughter chloroplasts.⁵²²

A remnant of the outer plastid dividing ring remains floating between the two daughter chloroplasts, and a remnant of the dynamin ring remains attached to one of the daughter chloroplasts.⁵²³

Of the five or six rings involved in chloroplast division, only the outer plastid-dividing ring is present for the entire constriction and division phase—while the Z-ring forms first, constriction does not begin until the outer plastid-dividing ring forms.⁵²⁴

Regulation

In species of algae that contain a single chloroplast, regulation of chloroplast division is extremely important to ensure that each daughter cell receives a chloroplast—chloroplasts can't be made from scratch.⁵²⁵ ⁵²⁶ In organisms like plants, whose cells contain multiple chloroplasts, coordination is looser and less important. It is likely that chloroplast and cell division are somewhat synchronized, though the mechanisms for it are mostly unknown.⁵²⁷

Light has been shown to be a requirement for chloroplast division. Chloroplasts can grow and progress through some of the constriction stages under poor quality green light, but are slow to complete division—they require exposure to bright white light to complete division. Spinach leaves grown under green light have been observed to contain many large dumbbell-shaped chloroplasts. Exposure to white light can stimulate these chloroplasts to divide and reduce the population of dumbbell-shaped chloroplasts.⁵²⁸ ⁵²⁹

Chloroplast inheritance

Like mitochondria, chloroplasts are usually inherited from a single parent. Biparental chloroplast inheritance—where plastid genes are inherited from both parent plants—occurs in very low levels in some flowering plants.⁵³⁰

Many mechanisms prevent biparental chloroplast DNA inheritance, including selective destruction of chloroplasts or their genes within the gamete or zygote, and chloroplasts from one parent being excluded from the embryo. Parental chloroplasts can be sorted so that only one type is present in each offspring.⁵³¹

Gymnosperms, such as pine trees, mostly pass on chloroplasts paternally,⁵³² while flowering plants often inherit chloroplasts maternally.⁵³³ ⁵³⁴ Flowering plants were once thought to only inherit chloroplasts maternally. However, there are now many documented cases of angiosperms inheriting chloroplasts paternally.⁵³⁵

Angiosperms, which pass on chloroplasts maternally, have many ways to prevent paternal inheritance. Most of them produce sperm cells that do not contain any plastids. There are many other documented mechanisms that prevent paternal inheritance in these flowering plants, such as different rates of chloroplast replication within the embryo.⁵³⁶

Among angiosperms, paternal chloroplast inheritance is observed more often in hybrids than in offspring from parents of the same species. This suggests that incompatible hybrid genes might interfere with the mechanisms that prevent paternal inheritance.⁵³⁷

Transplastomic plants

Recently, chloroplasts have caught attention by developers of genetically modified crops. Since, in most flowering plants, chloroplasts are not inherited from the male parent, transgenes in these plastids cannot be disseminated by pollen. This makes plastid transformation a valuable tool for the creation and cultivation of genetically modified plants that are biologically contained, thus posing significantly lower environmental risks. This biological containment strategy is therefore suitable for establishing the coexistence of conventional and organic agriculture. While the reliability of this mechanism has not yet been studied for all relevant crop species, recent results in tobacco plants are promising, showing a failed containment rate of transplastomic plants at 3 in 1,000,000.⁵³⁸

Footnotes

External links

Wikimedia Commons has media related to Chloroplasts.

Chloroplast – Cell Centered Database
Clegg MT, Gaut BS, Learn GH, Morton BR (July 1994). "Rates and patterns of chloroplast DNA evolution". Proceedings of the National Academy of Sciences of the United States of America. 91 (15): 6795–801. Bibcode:1994PNAS...91.6795C. doi:10.1073/pnas.91.15.6795. PMC 44285. PMID 8041699.
Co-Extra research on chloroplast transformation
NCBI full chloroplast genome

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Burgess J (1989). An introduction to plant cell development. Cambridge: Cambridge university press. p. 56. ISBN 0-521-31611-1. 0-521-31611-1 ↩
Burgess J (1989). An introduction to plant cell development. Cambridge: Cambridge university press. p. 56. ISBN 0-521-31611-1. 0-521-31611-1 ↩
Burgess J (1989). An introduction to plant cell development (Pbk. ed.). Cambridge: Cambridge university press. p. 57. ISBN 0-521-31611-1. 0-521-31611-1 ↩
Burgess J (1989). An introduction to plant cell development (Pbk. ed.). Cambridge: Cambridge university press. pp. 54–55. ISBN 0-521-31611-1. 0-521-31611-1 ↩
Possingham JV, Rose RJ (1976). "Chloroplast Replication and Chloroplast DNA Synthesis in Spinach Leaves". Proceedings of the Royal Society B: Biological Sciences. 193 (1112): 295–305. Bibcode:1976RSPSB.193..295P. doi:10.1098/rspb.1976.0047. S2CID 2691108. /wiki/Bibcode_(identifier) ↩
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Glynn JM, Miyagishima SY, Yoder DW, Osteryoung KW, Vitha S (May 2007). "Chloroplast division". Traffic. 8 (5): 451–61. doi:10.1111/j.1600-0854.2007.00545.x. PMID 17451550. S2CID 2808844. https://doi.org/10.1111%2Fj.1600-0854.2007.00545.x ↩
Burgess J (1989). An introduction to plant cell development (Pbk. ed.). Cambridge: Cambridge university press. pp. 54–55. ISBN 0-521-31611-1. 0-521-31611-1 ↩
Glynn JM, Miyagishima SY, Yoder DW, Osteryoung KW, Vitha S (May 2007). "Chloroplast division". Traffic. 8 (5): 451–61. doi:10.1111/j.1600-0854.2007.00545.x. PMID 17451550. S2CID 2808844. https://doi.org/10.1111%2Fj.1600-0854.2007.00545.x ↩
Miyagishima SY, Nishida K, Mori T, Matsuzaki M, Higashiyama T, Kuroiwa H, Kuroiwa T (March 2003). "A plant-specific dynamin-related protein forms a ring at the chloroplast division site". The Plant Cell. 15 (3): 655–65. Bibcode:2003PlanC..15..655M. doi:10.1105/tpc.009373. PMC 150020. PMID 12615939. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC150020 ↩
Glynn JM, Miyagishima SY, Yoder DW, Osteryoung KW, Vitha S (May 2007). "Chloroplast division". Traffic. 8 (5): 451–61. doi:10.1111/j.1600-0854.2007.00545.x. PMID 17451550. S2CID 2808844. https://doi.org/10.1111%2Fj.1600-0854.2007.00545.x ↩
Miyagishima SY, Nishida K, Mori T, Matsuzaki M, Higashiyama T, Kuroiwa H, Kuroiwa T (March 2003). "A plant-specific dynamin-related protein forms a ring at the chloroplast division site". The Plant Cell. 15 (3): 655–65. Bibcode:2003PlanC..15..655M. doi:10.1105/tpc.009373. PMC 150020. PMID 12615939. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC150020 ↩
Glynn JM, Miyagishima SY, Yoder DW, Osteryoung KW, Vitha S (May 2007). "Chloroplast division". Traffic. 8 (5): 451–61. doi:10.1111/j.1600-0854.2007.00545.x. PMID 17451550. S2CID 2808844. https://doi.org/10.1111%2Fj.1600-0854.2007.00545.x ↩
Glynn JM, Miyagishima SY, Yoder DW, Osteryoung KW, Vitha S (May 2007). "Chloroplast division". Traffic. 8 (5): 451–61. doi:10.1111/j.1600-0854.2007.00545.x. PMID 17451550. S2CID 2808844. https://doi.org/10.1111%2Fj.1600-0854.2007.00545.x ↩
Glynn JM, Miyagishima SY, Yoder DW, Osteryoung KW, Vitha S (May 2007). "Chloroplast division". Traffic. 8 (5): 451–61. doi:10.1111/j.1600-0854.2007.00545.x. PMID 17451550. S2CID 2808844. https://doi.org/10.1111%2Fj.1600-0854.2007.00545.x ↩
Miyagishima SY, Nishida K, Mori T, Matsuzaki M, Higashiyama T, Kuroiwa H, Kuroiwa T (March 2003). "A plant-specific dynamin-related protein forms a ring at the chloroplast division site". The Plant Cell. 15 (3): 655–65. Bibcode:2003PlanC..15..655M. doi:10.1105/tpc.009373. PMC 150020. PMID 12615939. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC150020 ↩
Glynn JM, Miyagishima SY, Yoder DW, Osteryoung KW, Vitha S (May 2007). "Chloroplast division". Traffic. 8 (5): 451–61. doi:10.1111/j.1600-0854.2007.00545.x. PMID 17451550. S2CID 2808844. https://doi.org/10.1111%2Fj.1600-0854.2007.00545.x ↩
Miyagishima SY, Nishida K, Mori T, Matsuzaki M, Higashiyama T, Kuroiwa H, Kuroiwa T (March 2003). "A plant-specific dynamin-related protein forms a ring at the chloroplast division site". The Plant Cell. 15 (3): 655–65. Bibcode:2003PlanC..15..655M. doi:10.1105/tpc.009373. PMC 150020. PMID 12615939. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC150020 ↩
Miyagishima SY, Nishida K, Mori T, Matsuzaki M, Higashiyama T, Kuroiwa H, Kuroiwa T (March 2003). "A plant-specific dynamin-related protein forms a ring at the chloroplast division site". The Plant Cell. 15 (3): 655–65. Bibcode:2003PlanC..15..655M. doi:10.1105/tpc.009373. PMC 150020. PMID 12615939. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC150020 ↩
Glynn JM, Miyagishima SY, Yoder DW, Osteryoung KW, Vitha S (May 2007). "Chloroplast division". Traffic. 8 (5): 451–61. doi:10.1111/j.1600-0854.2007.00545.x. PMID 17451550. S2CID 2808844. https://doi.org/10.1111%2Fj.1600-0854.2007.00545.x ↩
Miyagishima SY, Nishida K, Mori T, Matsuzaki M, Higashiyama T, Kuroiwa H, Kuroiwa T (March 2003). "A plant-specific dynamin-related protein forms a ring at the chloroplast division site". The Plant Cell. 15 (3): 655–65. Bibcode:2003PlanC..15..655M. doi:10.1105/tpc.009373. PMC 150020. PMID 12615939. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC150020 ↩
Hashimoto H, Possingham JV (April 1989). "Effect of light on the chloroplast division cycle and DNA synthesis in cultured leaf discs of spinach". Plant Physiology. 89 (4): 1178–83. doi:10.1104/pp.89.4.1178. PMC 1055993. PMID 16666681. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1055993 ↩
Miyagishima SY, Nishida K, Mori T, Matsuzaki M, Higashiyama T, Kuroiwa H, Kuroiwa T (March 2003). "A plant-specific dynamin-related protein forms a ring at the chloroplast division site". The Plant Cell. 15 (3): 655–65. Bibcode:2003PlanC..15..655M. doi:10.1105/tpc.009373. PMC 150020. PMID 12615939. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC150020 ↩
Glynn JM, Miyagishima SY, Yoder DW, Osteryoung KW, Vitha S (May 2007). "Chloroplast division". Traffic. 8 (5): 451–61. doi:10.1111/j.1600-0854.2007.00545.x. PMID 17451550. S2CID 2808844. https://doi.org/10.1111%2Fj.1600-0854.2007.00545.x ↩
Miyagishima SY, Nishida K, Mori T, Matsuzaki M, Higashiyama T, Kuroiwa H, Kuroiwa T (March 2003). "A plant-specific dynamin-related protein forms a ring at the chloroplast division site". The Plant Cell. 15 (3): 655–65. Bibcode:2003PlanC..15..655M. doi:10.1105/tpc.009373. PMC 150020. PMID 12615939. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC150020 ↩
Miyagishima SY, Nishida K, Mori T, Matsuzaki M, Higashiyama T, Kuroiwa H, Kuroiwa T (March 2003). "A plant-specific dynamin-related protein forms a ring at the chloroplast division site". The Plant Cell. 15 (3): 655–65. Bibcode:2003PlanC..15..655M. doi:10.1105/tpc.009373. PMC 150020. PMID 12615939. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC150020 ↩
Alberts B (2002). Molecular biology of the cell (4. ed.). New York [u.a.]: Garland. ISBN 0-8153-4072-9. 0-8153-4072-9 ↩
Glynn JM, Miyagishima SY, Yoder DW, Osteryoung KW, Vitha S (May 2007). "Chloroplast division". Traffic. 8 (5): 451–61. doi:10.1111/j.1600-0854.2007.00545.x. PMID 17451550. S2CID 2808844. https://doi.org/10.1111%2Fj.1600-0854.2007.00545.x ↩
Glynn JM, Miyagishima SY, Yoder DW, Osteryoung KW, Vitha S (May 2007). "Chloroplast division". Traffic. 8 (5): 451–61. doi:10.1111/j.1600-0854.2007.00545.x. PMID 17451550. S2CID 2808844. https://doi.org/10.1111%2Fj.1600-0854.2007.00545.x ↩
Possingham JV, Rose RJ (1976). "Chloroplast Replication and Chloroplast DNA Synthesis in Spinach Leaves". Proceedings of the Royal Society B: Biological Sciences. 193 (1112): 295–305. Bibcode:1976RSPSB.193..295P. doi:10.1098/rspb.1976.0047. S2CID 2691108. /wiki/Bibcode_(identifier) ↩
Hashimoto H, Possingham JV (April 1989). "Effect of light on the chloroplast division cycle and DNA synthesis in cultured leaf discs of spinach". Plant Physiology. 89 (4): 1178–83. doi:10.1104/pp.89.4.1178. PMC 1055993. PMID 16666681. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1055993 ↩
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Ruf S, Karcher D, Bock R (April 2007). "Determining the transgene containment level provided by chloroplast transformation". Proceedings of the National Academy of Sciences of the United States of America. 104 (17): 6998–7002. Bibcode:2007PNAS..104.6998R. doi:10.1073/pnas.0700008104. PMC 1849964. PMID 17420459. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1849964 ↩
Hansen AK, Escobar LK, Gilbert LE, Jansen RK (January 2007). "Paternal, maternal, and biparental inheritance of the chloroplast genome in Passiflora (Passifloraceae): implications for phylogenetic studies". American Journal of Botany. 94 (1): 42–6. doi:10.3732/ajb.94.1.42. PMID 21642206. /wiki/Doi_(identifier) ↩
Hansen AK, Escobar LK, Gilbert LE, Jansen RK (January 2007). "Paternal, maternal, and biparental inheritance of the chloroplast genome in Passiflora (Passifloraceae): implications for phylogenetic studies". American Journal of Botany. 94 (1): 42–6. doi:10.3732/ajb.94.1.42. PMID 21642206. /wiki/Doi_(identifier) ↩
Hansen AK, Escobar LK, Gilbert LE, Jansen RK (January 2007). "Paternal, maternal, and biparental inheritance of the chloroplast genome in Passiflora (Passifloraceae): implications for phylogenetic studies". American Journal of Botany. 94 (1): 42–6. doi:10.3732/ajb.94.1.42. PMID 21642206. /wiki/Doi_(identifier) ↩
Ruf S, Karcher D, Bock R (April 2007). "Determining the transgene containment level provided by chloroplast transformation". Proceedings of the National Academy of Sciences of the United States of America. 104 (17): 6998–7002. Bibcode:2007PNAS..104.6998R. doi:10.1073/pnas.0700008104. PMC 1849964. PMID 17420459. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1849964 ↩