List of C4 plants

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Maize (Zea mays, Poaceae) is the most widely cultivated C4 plant. A farmer in the foreground examining the stalks and looking at some ears of corn on some very tall plants, Ontario (20691586748).jpg
Maize ( Zea mays , Poaceae) is the most widely cultivated C4 plant.

In botany, C4 carbon fixation is one of three known methods of photosynthesis used by plants. C4 plants increase their photosynthetic efficiency by reducing or suppressing photorespiration, which mainly occurs under low atmospheric CO2 concentration, high light, high temperature, drought, and salinity. [2] [3] There are roughly 8,100 known C4 species, which belong to at least 61 distinct evolutionary lineages in 19 families (as per APG IV classification [4] ) of flowering plants. [1] Among these are important crops such as maize, sorghum and sugarcane, but also weeds and invasive plants. [1] Although only 3% of flowering plant species use C4 carbon fixation, they account for 23% of global primary production. [5] The repeated, convergent C4 evolution from C3 ancestors has spurred hopes to bio-engineer the C4 pathway into C3 crops such as rice. [1] [5]

Contents

C4 photosynthesis probably first evolved 30–35 million years ago in the Oligocene, and further origins occurred since, most of them in the last 15 million years. C4 plants are mainly found in tropical and warm-temperate regions, predominantly in open grasslands where they are often dominant. While most are graminoids, other growth forms such as forbs, vines, shrubs, and even some trees and aquatic plants are also known among C4 plants. [1]

C4 plants are usually identified by their higher 13C/12C isotopic ratio compared to C3 plants or their typical leaf anatomy. [5] The distribution of C4 lineages among plants has been determined through phylogenetics and was considered well known as of 2016. Monocots – mainly grasses (Poaceae) and sedges (Cyperaceae) – account for around 80% of C4 species, but they are also found in the eudicots. [1] Moreover, almost all C4 plants are herbaceus, with the notable exception of some woody species from the Euphorbia genus, such as the tree Euphorbia olowaluana . [6] The reason behind C4 metabolism extreme rarity in trees is debated: hypotheses vary from a possible reduction in photosynthetic quantum yield under dense canopy conditions, coupled with an increased metabolic energy consumption (inherent to C4 metabolism itself), to less efficient sunflecks utilization. [7]

The following list presents known C4 lineages by family, based on the overview by Sage (2016). [1] They correspond to single species or clades thought to have acquired the C4 pathway independently. In some lineages that also include C3 and C3–C4 intermediate species, the C4 pathway may have evolved more than once. [1]

Blepharis attenuata (Acanthaceae) grows in deserts. Blepharis attenuata 1.jpg
Blepharis attenuata (Acanthaceae) grows in deserts.
Shadscale (Atriplex confertifolia, Amaranthaceae) is a halophytic shrub common in steppes of western North America. Atriplex confertifolia (5063217522).jpg
Shadscale ( Atriplex confertifolia , Amaranthaceae) is a halophytic shrub common in steppes of western North America.
Black saxaul (Haloxylon ammodendron, Amaranthaceae) provided fuel for caravans following the Silk Road in Central Asia. Saxaul-baum.JPG
Black saxaul ( Haloxylon ammodendron , Amaranthaceae) provided fuel for caravans following the Silk Road in Central Asia.
Cleome gynandra (Cleomaceae) has been a C4 model plant. Starr 040323-0095 Cleome gynandra.jpg
Cleome gynandra (Cleomaceae) has been a C4 model plant.
Papyrus (Cyperus papyrus, Cyperaceae) has been of major cultural importance. Cyperus papyrus (Kafue River).jpg
Papyrus ( Cyperus papyrus , Cyperaceae) has been of major cultural importance.
Spotted spurge (Euphorbia maculata, Euphorbiaceae) commonly grows in sidewalk cracks in North America. Chamaesyce maculata (L.) Small (AM AK360262-3).jpg
Spotted spurge ( Euphorbia maculata , Euphorbiaceae) commonly grows in sidewalk cracks in North America.
The aquatic Egeria densa (Hydrocharitaceae) uses the C4 pathway under high temperature and light intensity. Egeria densa iceland.JPG
The aquatic Egeria densa (Hydrocharitaceae) uses the C4 pathway under high temperature and light intensity.
Sugarcane (Saccharum officinarum, Poaceae) is grown for sugar and bioethanol. Cana de Azucar.jpg
Sugarcane ( Saccharum officinarum , Poaceae) is grown for sugar and bioethanol.
Purslane (Portulaca oleracea, Portulacaceae), a weed and ancient vegetable, uses both C4 and CAM photosynthesis. 20150610Portulaca oleracea3.jpg
Purslane ( Portulaca oleracea , Portulacaceae), a weed and ancient vegetable, uses both C4 and CAM photosynthesis.
Rhodes grass (Chloris gayana, Poaceae) is a major forage grass in tropical areas. Chloris gayana habit4 (7069868575).jpg
Rhodes grass ( Chloris gayana , Poaceae) is a major forage grass in tropical areas.
The spiny fruits of puncture vine (Tribulus terrestris, Zygophyllaceae) may even puncture tyres. Starr 030612-0067 Tribulus terrestris.jpg
The spiny fruits of puncture vine ( Tribulus terrestris , Zygophyllaceae) may even puncture tyres.

Acanthaceae

The large acanthus family Acanthaceae includes one genus with C4 species, found in dry habitats from Africa to Asia. [10]

Aizoaceae

While many species in the ice plant family Aizoaceae use crassulacean acid metabolism (CAM), one subfamily with drought-tolerant and halophytic plants includes C4 species: [11]

Amaranthaceae

The amaranth family Amaranthaceae (including the former goosefoot family Chenopodiaceae) contains around 800 known C4 species, which belong to 14 distinct lineages in seven subfamilies. This makes Amaranthaceae the family with most C4 species and lineages among the eudicots. [1] Suaeda aralocaspica and species of the genus Bienertia use a particular, single-cell type of C4 carbon fixation. [1] [12]

Asteraceae

The composite family Asteraceae contains three C4 lineages, in two different tribes of subfamily Asteroideae. [1] [20] They include the model genus Flaveria with closely related C3, C4, and intermediate species. [1]

Boraginaceae

The borage family Boraginaceae contains one widespread C4 genus, Euploca, which has also been treated as part of a distinct family Heliotropiaceae. [24]

Cleomaceae

The Cleomaceae, formerly included in the caper family Capparaceae, contains three C4 species in genus Cleome . These three species independently acquired the C4 pathway; the genus also contains numerous C3 as well as C3–C4 intermediate species. [1] [26] [27]

Caryophyllaceae

In the carnation family Caryophyllaceae, the C4 pathway evolved once, in a clade within the polyphyletic genus Polycarpaea. [1] [28]

Cyperaceae

The sedge family Cyperaceae is second only to the grasses in number of C4 species. Prominent C4 sedges include culturally important species such as papyrus ( Cyperus papyrus ) and chufa ( C. esculentus ) but also purple nutsedge ( C. rotundus ), one of the world's major weeds. Eleocharis vivipara uses C3 carbon fixation in underwater leaves and C4 carbon fixation in aerial leaves. [1]

Euphorbiaceae

The spurge family Euphorbiaceae contains the largest single C4 lineage among eudicots. The C4 spurges are diverse and widespread; they range from weedy herbs to the only known C4 trees – four species from Hawaii, including Euphorbia olowaluana (up to 10 m) and E. herbstii (up to 8 m). [1] [8]

Gisekiaceae

Contains a C4 genus with a single species.

Hydrocharitaceae

Includes the only known aquatic C4 plants. [1]

Molluginaceae

The two C4 species within the same genus have acquired the pathway independently.

Nyctaginaceae

Polygonaceae

Portulacaceae

The single genus of this family forms one C4 lineage. CAM photosynthesis is also known. Common purslane ( Portulaca oleracea ) is a major weed but also a vegetable. [1]

Poaceae

The grass family includes most of the known C4 species – around 5000. They are only found in subfamilies of the PACMAD clade. Major C4 crops such as maize, sugarcane, sorghum and pearl millet belong in this family. The only known species with C3, C4 and intermediate variants, Alloteropsis semialata , is a grass. [1]

Scrophulariaceae

Zygophyllaceae

Related Research Articles

<span class="mw-page-title-main">Amaranthaceae</span> Family of flowering plants

Amaranthaceae is a family of flowering plants commonly known as the amaranth family, in reference to its type genus Amaranthus. It includes the former goosefoot family Chenopodiaceae and contains about 165 genera and 2,040 species, making it the most species-rich lineage within its parent order, Caryophyllales.

<span class="mw-page-title-main">Crassulacean acid metabolism</span> Metabolic process

Crassulacean acid metabolism, also known as CAM photosynthesis, is a carbon fixation pathway that evolved in some plants as an adaptation to arid conditions that allows a plant to photosynthesize during the day, but only exchange gases at night. In a plant using full CAM, the stomata in the leaves remain shut during the day to reduce evapotranspiration, but they open at night to collect carbon dioxide and allow it to diffuse into the mesophyll cells. The CO2 is stored as four-carbon malic acid in vacuoles at night, and then in the daytime, the malate is transported to chloroplasts where it is converted back to CO2, which is then used during photosynthesis. The pre-collected CO2 is concentrated around the enzyme RuBisCO, increasing photosynthetic efficiency. This mechanism of acid metabolism was first discovered in plants of the family Crassulaceae.

C<sub>4</sub> carbon fixation Photosynthetic process in some plants

C4 carbon fixation or the Hatch–Slack pathway is one of three known photosynthetic processes of carbon fixation in plants. It owes the names to the 1960s discovery by Marshall Davidson Hatch and Charles Roger Slack.

<span class="mw-page-title-main">Paulowniaceae</span> Family of trees

Paulowniaceae are a family of flowering plants within the Lamiales. They are a monophyletic and monogeneric family of trees with currently 7 confirmed species. They were formerly placed within Scrophulariaceae sensu lato, or as a segregate of the Bignoniaceae.

<span class="mw-page-title-main">Salicornioideae</span> Subfamily of flowering plants

The Salicornioideae are a subfamily of the flowering plant family Amaranthaceae. Important characters are succulent, often articulated stems, strongly reduced leaves, and flowers aggregated in thick, dense spike-shaped thyrses. These halophytic plants are distributed worldwide. Many are edible

<span class="mw-page-title-main">Gomphrenoideae</span> Subfamily of flowering plants

The Gomphrenoideae are a subfamily of the Amaranthaceae.

<i>Atriplex</i> Genus of flowering plant

Atriplex is a plant genus of about 250 species, known by the common names of saltbush and orache. It belongs to the subfamily Chenopodioideae of the family Amaranthaceae s.l.. The genus is quite variable and widely distributed. It includes many desert and seashore plants and halophytes, as well as plants of moist environments. The generic name originated in Latin and was applied by Pliny the Elder to the edible oraches. The name saltbush derives from the fact that the plants retain salt in their leaves; they are able to grow in areas affected by soil salination.

<span class="mw-page-title-main">Panicoideae</span> Subfamily of plants

Panicoideae is the second-largest subfamily of the grasses with over 3,500 species, mainly distributed in warm temperate and tropical regions. It comprises some important agricultural crops, including sugarcane, maize, sorghum, and switchgrass.

<i>Chamaesyce</i> Genus of flowering plants

Chamaesyce is a subgenus of plants in the family Euphorbiaceae. Recent phylogenetic studies have shown that Chamaesyce is deeply nested within the broader Euphorbia. Specifically, Chamaesyce is very closely related to plants like Euphorbia pulcherrima, the popular poinsettia. Currently, all species have now been reclassified as species of Euphorbia. Specifically, this group now belongs to Euphorbia subgenus Chamaesyce section Anisophyllum. Taxonomically speaking, Chamaesyce is considered a synonym of Euphorbia.

<i>Suaeda</i> Genus of aquatic plants

Suaeda is a genus of plants also known as seepweeds and sea-blites. Most species are confined to saline or alkaline soil habitats, such as coastal salt-flats and tidal wetlands. Many species have thick, succulent leaves, a characteristic seen in various plant genera that thrive in salty habitats.

<i>Aerva</i> Genus of flowering plants

Aerva is a genus of plants in the family Amaranthaceae. Its species are native to the palaeotropics, throughout continental Africa, Madagascar and smaller islands, through parts of the Middle East, India, and southeast Asia. Aerva javanica is an alien in northern Australia.

<i>Flaveria</i> Genus of flowering plants

Flaveria is a genus of plants in the family Asteraceae. They are sometimes called yellowtops. Some are annual or perennial herbs and some are shrubs. They bear yellow flowers in heads, with zero, one, or two ray florets in each head. These plants are found in the Americas, Asia, Africa, and Australia.

<i>Alloteropsis</i> Genus of grasses

Alloteropsis is a genus of Old World plants in the grass family.

Suaeda aralocaspica is a species of plant in the family Amaranthaceae that is restricted to the deserts of Central Asia. It is a halophyte and uses C4 carbon fixation but lacks the characteristic leaf anatomy of other C4 plants (known as kranz anatomy). Carrying out complete C4 photosynthesis within individual cells, these plants instead are known as single‐cell C4 system or SCC4 plants. This makes them distinct from typical C4 plants, which require the collaboration of two types of photosynthetic cells. SCC4 plants have features that make them potentially valuable in engineering higher photosynthetic efficiencies in agriculturally important C3 carbon fixation species such as rice. To address this, the 467 Mb genome of S. aralocaspica has been sequenced to help understanding of the evolution of SCC4 photosynthesis and contribute to the engineering of C4 photosynthesis into other economically important crops.

<span class="mw-page-title-main">Camphorosmeae</span> Tribe of flowering plants

Camphorosmeae is a species-rich tribe of the Amaranthaceae, formerly Chenopodiaceae, with 20 genera and about 179 species. It is classified as a single tribe of subfamily Camphorosmoideae.

<span class="mw-page-title-main">Suaedoideae</span> Subfamily of flowering plants

The Suaedoideae are a subfamily of plants in the family Amaranthaceae.

<i>Bienertia</i> Genus of plant in the family Amaranthaceae

Bienertia is a flowering plant genus that currently is classified in the family Amaranthaceae s.l.. For long time, the genus was considered to consist only of one species, Bienertia cycloptera, but in 2005 and 2012, two new species have been separated.

<span class="mw-page-title-main">Rhinantheae</span> Tribe of flowering plants in the broomrape family Orobanchaceae

Rhinantheae is a tribe with fewer than 20 genera of herbaceous plants in the family Orobanchaceae.

Elizabeth Anne Kellogg is an American botanist who now works mainly on grasses and cereals, both wild and cultivated. She earned a Ph.D. from Harvard University in 1983, and was professor of Botanical Studies at the University of Missouri - St. Louis from September 1998 to December 2013. Since 2013 she has been part of the Kellogg Lab at the Donald Danforth Plant Science Center in Missouri, where she is principal investigator In 2020 she was elected a member of the National Academy of Sciences.

Hedbergia longiflora, formerly Bartsia longiflora, is a species of flowering plants in the family Orobanchaceae.

References

  1. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 Sage, R.F. (2016). "A portrait of the C4 photosynthetic family on the 50th anniversary of its discovery: species number, evolutionary lineages, and Hall of Fame". Journal of Experimental Botany. 67 (14): 4039–4056. doi: 10.1093/jxb/erw156 . ISSN   0022-0957. PMID   27053721. Open Access logo PLoS transparent.svg
  2. ↑ Sage, R.F.; Sage, T.L.; Kocacinar, F. (2012). "Photorespiration and the evolution of C4 photosynthesis". Annual Review of Plant Biology. 63 (1): 19–47. doi:10.1146/annurev-arplant-042811-105511. ISSN   1543-5008. PMID   22404472.
  3. ↑ Christin, P.-A.; Osborne, C.P. (2014). "The evolutionary ecology of C4 plants" (PDF). New Phytologist. 204 (4): 765–781. doi: 10.1111/nph.13033 . ISSN   0028-646X. PMID   25263843. Open Access logo PLoS transparent.svg
  4. ↑ Angiosperm Phylogeny Group (2016). "An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV". Botanical Journal of the Linnean Society. 181 (1): 1–20. doi: 10.1111/boj.12385 . Open Access logo PLoS transparent.svg
  5. 1 2 3 Kellogg, E.A. (2013). "C4 photosynthesis". Current Biology. 23 (14): R594–R599. doi: 10.1016/j.cub.2013.04.066 . ISSN   0960-9822. PMID   23885869. Open Access logo PLoS transparent.svg
  6. ↑ Elliott, Liam (2020-05-22). "To C4 or not to C4 if you're a tree? Some possible answers". Botany One. Retrieved 2024-04-30.
  7. ↑ Young, Sophie N R.; Sack, Lawren; Sporck-Koehler, Margaret J.; Lundgren, Marjorie R. (2020). "Why is C4 photosynthesis so rare in trees?". Journal of Experimental Botany. 71 (16): 4629–4638. doi:10.1093/jxb/eraa234. PMC   7410182 . PMID   32409834 . Retrieved 2024-05-01.
  8. 1 2 Yang, Y.; Berry, P.E. (2011). "Phylogenetics of the Chamaesyce clade (Euphorbia, Euphorbiaceae): Reticulate evolution and long-distance dispersal in a prominent C4 lineage" (PDF). American Journal of Botany. 98 (9): 1486–1503. doi:10.3732/ajb.1000496. hdl: 2027.42/142099 . ISSN   0002-9122. PMID   21875975. Open Access logo PLoS transparent.svg
  9. ↑ Koch, K. E.; Kennedy, R. A. (1982). "Crassulacean acid metabolism in the succulent C4 dicot, Portulaca oleracea L. under natural environmental conditions". Plant Physiology. 69 (4): 757–761. doi:10.1104/pp.69.4.757. ISSN   0032-0889. PMC   426300 . PMID   16662291. Open Access logo PLoS transparent.svg
  10. ↑ Fisher, A.E.; McDade, L.A.; Kiel, C.A.; et al. (2015). "Evolutionary history of Blepharis (Acanthaceae) and the origin of C4 photosynthesis in section Acanthodium". International Journal of Plant Sciences. 176 (8): 770–790. doi:10.1086/683011. ISSN   1058-5893. Open Access logo PLoS transparent.svg
  11. ↑ Bohley, K.; Joos, O.; Hartmann, H.; et al. (2015). "Phylogeny of Sesuvioideae (Aizoaceae) – biogeography, leaf anatomy and the evolution of C4 photosynthesis". Perspectives in Plant Ecology, Evolution and Systematics. 17 (2): 116–130. doi:10.1016/j.ppees.2014.12.003. ISSN   1433-8319.
  12. 1 2 3 4 5 Schütze, P.; Freitag, H.; Weising, K. (2003). "An integrated molecular and morphological study of the subfamily Suaedoideae Ulbr. (Chenopodiaceae)". Plant Systematics and Evolution. 239 (3–4): 257–286. Bibcode:2003PSyEv.239..257S. doi:10.1007/s00606-003-0013-2. ISSN   0378-2697. S2CID   20250636.
  13. 1 2 3 4 5 Sage, R.F.; Sage, T.L.; Pearcy, R.W.; Borsch, T. (2007). "The taxonomic distribution of C4 photosynthesis in Amaranthaceae sensu stricto". American Journal of Botany. 94 (12): 1992–2003. doi:10.3732/ajb.94.12.1992. ISSN   0002-9122. PMID   21636394. Open Access logo PLoS transparent.svg
  14. ↑ Kadereit, G.; Mavrodiev, E.V.; Zacharias, E.H.; Sukhorukov, A.P. (2010). "Molecular phylogeny of Atripliceae (Chenopodioideae, Chenopodiaceae): Implications for systematics, biogeography, flower and fruit evolution, and the origin of C4 photosynthesis". American Journal of Botany. 97 (10): 1664–1687. doi:10.3732/ajb.1000169. ISSN   0002-9122. PMID   21616801. Open Access logo PLoS transparent.svg
  15. ↑ Kadereit, G.; Freitag, H. (2011). "Molecular phylogeny of Camphorosmeae (Camphorosmoideae, Chenopodiaceae): Implications for biogeography, evolution of C4-photosynthesis and taxonomy". Taxon. 60 (1): 51–78. doi:10.1002/tax.601006.
  16. ↑ Kapralov, M.V.; Akhani, H.; Voznesenskaya, E.V.; Edwards, G.; Franceschi, V.; Roalson, E.H. (2006). "Phylogenetic Relationships in the Salicornioideae / Suaedoideae / Salsoloideae s.l. (Chenopodiaceae) clade and a clarification of the phylogenetic position of Bienertia and Alexandra using multiple DNA sequence datasets". Systematic Botany. 31 (3): 571–585. doi:10.1600/036364406778388674. ISSN   0363-6445.
  17. 1 2 Pyankov, V.; Ziegler, H.; Kuz'min, A.; Edwards, G. (2001). "Origin and evolution of C4 photosynthesis in the tribe Salsoleae (Chenopodiaceae) based on anatomical and biochemical types in leaves and cotyledons". Plant Systematics and Evolution. 230 (1–2): 43–74. Bibcode:2001PSyEv.230...43P. doi:10.1007/s006060170004. ISSN   0378-2697. S2CID   25370346.
  18. 1 2 Akhani, H.; Edwards, G.; Roalson, E.H. (2007). "Diversification of the Old World Salsoleae s.l. (Chenopodiaceae): Molecular phylogenetic analysis of nuclear and chloroplast data sets and a revised classification". International Journal of Plant Sciences. 168 (6): 931–956. doi:10.1086/518263. ISSN   1058-5893.
  19. ↑ Voznesenskaya, E.V.; Akhani, H.; Koteyeva, N.K.; et al. (2008). "Structural, biochemical, and physiological characterization of photosynthesis in two C4 subspecies of Tecticornia indica and the C3 species Tecticornia pergranulata (Chenopodiaceae)". Journal of Experimental Botany. 59 (7): 1715–1734. doi: 10.1093/jxb/ern028 . ISSN   1460-2431. PMID   18390850.
  20. 1 2 Kellogg, E.A. (1999). "Phylogenetic aspects of the evolution of C4 photosynthesis" (PDF). In Sage, R.F.; Monson, R.K. (eds.). C4 plant biology. San Diego, CA: Academic Press. pp. 411–44. ISBN   978-0126144406 . Retrieved 2018-05-26.
  21. ↑ McKown, A.D.; Moncalvo, J.-M.; Dengler, N.G. (2005). "Phylogeny of Flaveria (Asteraceae) and inference of C4 photosynthesis evolution". American Journal of Botany. 92 (11): 1911–1928. doi: 10.3732/ajb.92.11.1911 . ISSN   0002-9122. PMID   21646108. Open Access logo PLoS transparent.svg
  22. ↑ Lyu, M.-J.A.; Gowik, U.; Kelly, S.; et al. (2015). "RNA-Seq based phylogeny recapitulates previous phylogeny of the genus Flaveria (Asteraceae) with some modifications". BMC Evolutionary Biology. 15 (1): 116. Bibcode:2015BMCEE..15..116L. doi: 10.1186/s12862-015-0399-9 . ISSN   1471-2148. PMC   4472175 . PMID   26084484. Open Access logo PLoS transparent.svg
  23. ↑ Hansen, D.R. (2012). The molecular phylogeny of Pectis L. (Tageteae, Asteraceae), with implications for taxonomy, biogeography, and the evolution of C4 photosynthesis (Doctoral dissertation). University of Texas, Austin. Retrieved 2018-05-27. Open Access logo PLoS transparent.svg
  24. ↑ Luebert, F.; Cecchi, L.; Frohlich, M.W.; Gottschling, M.; Guilliams, C.M.; Hasenstab-Lehman, K.E.; Hilger, H.H.; Miller, J.S.; Mittelbach, M.; Nazaire, M.; Nepi, M.; Nocentini, D.; Ober, D.; Olmstead, R.G.; Selvi, F.; Simpson, M.G.; Sutorý, K.; Valdés, B.; Walden, G.K.; Weigend, M. (2016). "Familial classification of the Boraginales". Taxon. 65 (3): 502–522. doi:10.12705/653.5. hdl: 2158/1062790 . ISSN   0040-0262 . Retrieved 16 June 2018.
  25. ↑ Vogan, P.J.; Frohlich, M.W.; Sage, R.F. (2007). "The functional significance of C3–C4 intermediate traits in Heliotropium L. (Boraginaceae): gas exchange perspectives". Plant, Cell & Environment. 30 (10): 1337–1345. doi: 10.1111/j.1365-3040.2007.01706.x . ISSN   0140-7791. PMID   17727423. Open Access logo PLoS transparent.svg
  26. ↑ Marshall, D.M.; Muhaidat, R.; Brown, N.J.; et al. (2007). "Cleome, a genus closely related to Arabidopsis, contains species spanning a developmental progression from C3 to C4 photosynthesis". The Plant Journal. 51 (5): 886–896. doi: 10.1111/j.1365-313X.2007.03188.x . ISSN   0960-7412. PMID   17692080. Open Access logo PLoS transparent.svg
  27. ↑ Feodorova, T.A.; Voznesenskaya, E.V.; Edwards, G.E.; Roalson, E.H. (2010). "Biogeographic patterns of diversification and the origins of C4 in Cleome (Cleomaceae)" (PDF). Systematic Botany. 35 (4): 811–826. doi:10.1600/036364410X539880. ISSN   0363-6445. S2CID   84983697 . Retrieved 16 June 2016.
  28. ↑ Kool, A. (2012). Desert plants and deserted islands: systematics and ethnobotany in Caryophyllaceae (PhD thesis). Uppsala University. pp. 35–36. ISBN   978-91-554-8471-2 . Retrieved 23 June 2018. Open Access logo PLoS transparent.svg
  29. ↑ Bissinger, K.; Khoshravesh, R.; Kotrade, J.P.; et al. (2014). "Gisekia (Gisekiaceae): Phylogenetic relationships, biogeography, and ecophysiology of a poorly known C4 lineage in the Caryophyllales". American Journal of Botany. 101 (3): 499–509. doi:10.3732/ajb.1300279. ISSN   0002-9122. PMID   24638165. Open Access logo PLoS transparent.svg
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