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Research Articles

Kranz anatomical and biochemical characterization of C4 photosynthesis in an aphyllous shrub Calligonum comosum (Polygonaceae)

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Pages 796-807 | Received 26 Dec 2023, Accepted 23 May 2024, Published online: 20 Jun 2024

References

  • Akhani H, Ghasemkhani M, Chuong SDX, Edwards GE. 2008. Occurrence and forms of Kranz anatomy in photosynthetic organs and characterization of NAD-ME subtype C4 photosynthesis in Blepharis ciliaris (L.) B.L. Burtt (Acanthaceae). J Exp Bot. 59(7):1755–1765. doi: 10.1093/jxb/ern020.
  • Akhani H, Trimborn P, Ziegler H. 1997. Photosynthetic pathways in Chenopodiaceae from Africa, Asia and Europe with their ecological, phytogeographical and taxonomical importance. Plant Syst Evol. 206:187–221.
  • Butnik AA, Matyunina TE, Abdullaeya AT, Nigmanova RN. 2016. Adaptation of assimilating organs Calligonum L. species (Polygonaceae Juss.) in Kyzylkum desert. JNASCI. 5:99–104.
  • Carolin RC, Jacobs SWL, Vesk M. 1975. Leaf structure in Chenopodiaceae. Bot Jahrb Syst. 95:226–255.
  • Danila FR, Quick WP, White RG, Furbank RT, von Caemmerer S. 2016. The metabolite pathway between bundle sheath and mesophyll: quantification of plasmodesmata in leaves of C3 and C4 monocots. Plant Cell. 28(6):1461–1471. doi: 10.1105/tpc.16.00155.
  • Danila FR, Quick WP, White RG, Kelly S, von Caemmerer S, Furbank RT. 2018. Multiple mechanisms for enhanced plasmodesmata density in disparate subtypes of C4 grasses. J Exp Bot. 69(5):1135–1145. doi: 10.1093/jxb/erx456.
  • Dengler NG, Nelson T. 1999. Leaf structure and development in C4 plants. In: Sage RF, Monson RK, editors. C4 plant biology, physiological ecology series. San Diego (CA): Academic Press; p. 133–172.
  • Doostmohammadi M, Malekmohammadi M, Djamali M, Akhani H. 2020. Is Pteropyrum a pathway to C4 evolution in Polygonaceae? An integrative approach to the taxonomy and anatomy of Pteropyrum (C3), an immediate relative of Calligonum (C4). Bot J Linn Soc. 192(2):369–400. doi: 10.1093/botlinnean/boz079.
  • Edwards GE, Franceschi VR, Ku MSB, Voznesenskaya EV, Pyankov VI, Andreo CS. 2001. Compartmentation of photosynthesis in cells and tissues of C4 plants. J Exp Bot. 52(356):577–590. doi: 10.1093/jexbot/52.356.577.
  • Edwards GE, Voznesenskaya EV. 2011. C4 photosynthesis: Kranz forms and single-cell C4 in terrestrial plants. In: Raghavendra AS, Sage RF, editors. C4 photosynthesis and related CO2 concentrating mechanisms. Dordrecht (the Netherlands): Springer; p. 29–61.
  • Fan Y, Asao S, Furbank RT, von Caemmerer S, Day DA, Tcherkez G, Sage TL, Sage RF, Atkin OK. 2022. The crucial roles of mitochondria in supporting C4 photosynthesis. New Phytol. 233(3):1083–1096. doi: 10.1111/nph.17818.
  • Freitag H, Kadereit G. 2014. C3 and C4 leaf anatomy types in Camphorosmeae (Camphorosmoideae, Chenopodiaceae). Plant Syst Evol. 300(4):665–687. doi: 10.1007/s00606-013-0912-9.
  • Gouja H, Fernández AG, Garnatje T, Raies A, Neffati M. 2014. Genome size and phylogenetic relationships between the Tunisian species of the genus Calligonum (Polygonaceae). Turk J Bot. 38:13–21. doi: 10.3906/bot-1301-72.
  • Jacobs SWL. 2001. Review of leaf anatomy and ultrastructure in the Chenopodiaceae (Caryophyllales). J Torrey Bot Soc. 128(3):236–253. doi: 10.2307/3088716.
  • Kadereit G, Borsch T, Weising K, Freitag H. 2003. Phylogeny of Amaranthaceae and Chenopodiaceae and the evolution of C4 photosynthesis. Int J Plant Sci. 164:959–986.
  • Kadereit G, Lauterbach M, Pirie MD, Arafeh R, Freitag H. 2014. When do different C4 leaf anatomies indicate independent C4 origins? Parallel evolution of C4 leaf types in Camphorosmeae (Chenopodiaceae). J Exp Bot. 65(13):3499–3511. doi: 10.1093/jxb/eru169.
  • Kanai R, Edwards GE. 1999. The biochemistry of C4 photosynthesis. In: Sage RF, Monson RK, editors. C4 plant biology, physiological ecology series. San Diego (CA): Academic Press; p. 87.
  • Koteyeva NK, Voznesenskaya EV, Berry JO, Chuong SDX, Franceschi VR, Edwards GE. 2011. Development of structural and biochemical characteristics of C4 photosynthesis in two types of Kranz anatomy in genus Suaeda (family Chenopodiaceae). J Exp Bot. 62(9):3197–3212. doi: 10.1093/jxb/err021.
  • Koteyeva NK, Voznesenskaya EV, Pathare VS, Borisenko TA, Zhurbenko PM, Morozov GA, Edwards GE. 2023. Biochemical and structural diversification of C4 photosynthesis in Tribe Zoysieae (Poaceae). Plants. 12(23):4049. doi: 10.3390/plants12234049.
  • Leegood RC, Walker RP. 2003. Regulation and roles of phosphoenolpyruvate carboxykinase in plants. Arch Biochem Biophys. 414:204–210.
  • Ludwig M. 2016. The roles of organic acids in C4 photosynthesis. Front Plant Sci. 7:647. doi: 10.3389/fpls.2016.00647.
  • Marshall DM, Muhaidat R, Brown NJ, Liu Z, Stanley S, Griffiths H, Sage RF, Hibberd JM. 2007. Cleome, a genus closely related to Arabidopsis, contains species spanning a developmental progression from C3 to C4 photosynthesis. Plant J. 51:886–896.
  • Muhaidat R, McKown AD. 2013. Significant involvement of PEP-CK in carbon assimilation of C4 eudicots. Ann Bot. 111(4):577–589. doi: 10.1093/aob/mct017.
  • Muhaidat R, McKown AD, Al Zoubi M, Bani DZ, Otoum O. 2018. C4 photosynthesis and transition of Kranz anatomy in cotyledons and leaves of Tetraena simplex. Am J Bot. 105(5):822–835. doi: 10.1002/ajb2.1087.
  • Muhaidat R, McKown AD, Khateeb W, Al A-SM, Domi Z, Hussein E, El-Oqlah AA. 2012. Full assessment of C4 photosynthesis in Blepharis attenuata Napper (Acanthaceae) from Jordan: evidence from leaf anatomy and key C4 photosynthetic enzymes. Asian J Plant Sci. 11:206–216.
  • Muhaidat R, Sage RF, Dengler NG. 2007. Diversity of Kranz anatomy and biochemistry in C4 eudicots. Am J Bot. 94(3):362–381. doi: 10.3732/ajb.94.3.362.
  • Munekage YN, Taniguchi YY. 2016. Promotion of cyclic electron transport around photosystem I with the development of C4 photosynthesis. Plant Cell Physiol. 57(5):897–903. doi: 10.1093/pcp/pcw012.
  • Purohit CS, Kumar R. 2020. A review on genus Calligonum L. (Polygonaceae) from India and report Calligonum crinitum an addition for Flora of India. J Asia Pac Biodivers. 13:319–324.
  • Pyankov VI, Black CC, Artyusheva EG, Voznesenskaya EV, Ku MSB, Edwards GE. 1999. Features of photosynthesis in Haloxylon species of Chenopodiaceae that are dominant plants in Central Asian deserts. Plant Cell Physiol. 40:125–134.
  • Pyankov VI, Gunin PD, Tsoog S, Black CC. 2000. C4 plants in the vegetation of Mongolia: their natural occurrence and geographical distribution in relation to climate. Oecologia. 123(1):15–31. doi: 10.1007/s004420050985.
  • Pyankov VI, Vakhrusheva DV, Seidova RD. 1994. Structure of the assimilation apparatus of plants of the genus Calligonum in relation to ecological conditions and uses for phytoamelioration in the arid zone. Probl Desert Dev. 1:41–49.
  • Pyankov VI, 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 Syst Evol. 230:43–74.
  • Rudov A, Mashkour M, Djamali M, Akhani H. 2020. A review of C4 plants in southwest Asia: an ecological, geographical and taxonomical analysis of a region with high diversity of C4 eudicots. Front Plant Sci. 11:546518. doi: 10.3389/fpls.2020.546518.
  • Safronova I. 2000. Ecological classification of shrubs and semi-shrubs in temperate deserts of Eurasia. In: Safronova IN, Yurkovskaya TK, editors. IAVS 2001. Proceedings of the 43d IAVS Symposium, July 23—28, vol. 1. Nagano, Japan: Vegetation of Russia; p. 77–78.
  • Sage RF. 2004. The evolution of C4 photosynthesis. New Phytol. 161(2):341–370. doi: 10.1111/j.1469-8137.2004.00974.x.
  • Sage RF. 2016. A portrait of the C4 photosynthetic family on the 50th anniversary of its discovery: species number, evolutionary lineages, and Hall of Fame. J Exp Bot. 68:e11–e28.
  • Sage RF. 2021. Russ Monson and the evolution of C4 photosynthesis. Oecologia. 197(4):823–840. doi: 10.1007/s00442-021-04883-1.
  • Sage RF, Christin P-A, Edwards EJ. 2011. The C4 plant lineages of planet Earth. J Exp Bot. 62(9):3155–3169. doi: 10.1093/jxb/err048.
  • Sage RF, Monson RK, Ehleringer JR, Adachi S, Pearcy RW. 2018. Some like it hot: the physiological ecology of C4 plant evolution. Oecologia. 187(4):941–966. doi: 10.1007/s00442-018-4191-6.
  • Sage RF, Sage TL, Kocacinar F. 2012. Photorespiration and the evolution of C4 photosynthesis. Annu Rev Plant Biol. 63:19–47. doi: 10.1146/annurev-arplant-042811-105511.
  • Sage RF, Sultmanis S. 2016. Why are there no C4 forests? J Plant Physiol. 20(203):55–68.
  • Sage RF, Wedin DA, Li MR. 1999. The biogeography of C4 photosynthesis: patterns and controlling factors. In: Sage RF, Monson RK, editors. The biology of C4 photosynthesis. San Diego (CA): Academic Press; p. 313–375.
  • Schreier TB, Müller KH, Eicke S, Faulkner C, Zeeman SC, Hibberd JM. 2023. Plasmodesmal connectivity in C4Gynandropsis gynandra is induced by light and dependent on photosynthesis. New Phytol. 241(1):298–313. doi: 10.1111/nph.19343.
  • Schüssler C, Freitag H, Koteyeva N, Schmidt D, Edwards G, Voznesenskaya E, Kadereit G. 2017. Molecular phylogeny and forms of photosynthesis in tribe Salsoleae (Chenopodiaceae). J Exp Bot. 68(2):207–223. doi: 10.1093/jxb/erw432.
  • Sharwood RE, Sonawane BV, Ghannoum O, Whitney SM. 2016. Improved analysis of C4 and C3 photosynthesis via refined in vitro assays of their carbon fixation biochemistry. J Exp Bot. 67(10):3137–3148. doi: 10.1093/jxb/erw154.
  • Soliman S, Mohammad MG, El-Keblawy AA, Omar H, Abouleish M, Madkour M, Elnaggar A, Hosni RM. 2018. Mechanical and phytochemical protection mechanisms of Calligonum comosum in arid deserts. PLoS One. 13(2):e0192576. doi: 10.1371/journal.pone.0192576.
  • Sudderth EA, Muhaidat RM, McKown AD, Kocacinar F, Sage RF. 2007. Leaf anatomy, gas exchange and photosynthetic enzyme activity in Flaveria kochiana. Funct Plant Biol. 34(2):118–129. doi: 10.1071/FP06263.
  • Stata M, Sage TL, Sage RF. 2019. Mind the gap: the evolutionary engagement of the C4 metabolic cycle in support of net carbon assimilation. Curr Opin Plant Biol. 49:27–34. doi: 10.1016/j.pbi.2019.04.008.
  • Taia WK, El-Etaby MO. 2006. Taxonomical study in the desert plant Calligonum comosum L’Her from two different locations in Saudi Arabia. Asian J Plant Sci. 5: 570–579.
  • Takabayashi A, Kishine M, Asada K, Endo T, Sato F. 2005. Differential use of two cyclic electron flows around photosystem I for driving CO2-concentration mechanism in C4 photosynthesis. Proc Natl Acad Sci. 102: 16898–16903.
  • Taniguchi M, Cousins AB. 2018. Significance of C4 leaf structure at the tissue and cellular levels. In: Adams III WW, Terashima I, editors. The leaf: a platform for performing photosynthesis. Advances in photosynthesis and respiration, vol. 44. New York: Springer, Cham; p. 255–279. doi: 10.1007/978-3-319-93594-2_9.
  • The Plant List. 2012. Version 1.1. [accessed 2021 Apr 2]. http://www.theplantlist.org/.
  • Von Caemmerer S, Furbank RT. 2003. The C4 pathway: an efficient CO2 pump. Photosynth Res. 77(2-3):191–207. doi: 10.1023/A:1025830019591.
  • Voznesenskaya EV, Franceschi VR, Pyankov VI, Edwards GE. 1999. Anatomy, chloroplast structure and compartmentation of enzymes relative to photosynthetic mechanisms in leaves and cotyledons of species in the tribe Salsoleae (Chenopodiaceae). J Exp Bot. 50(341):1779–1795. doi: 10.1093/jexbot/50.341.1779.
  • Voznesenskaya EV, Koteyeva NK, Edwards GE, Ocampo G. 2010. Revealing diversity in structural and biochemical forms of C4 photosynthesis and a C3–C4 intermediate in genus Portulaca L. (Portulacaceae). J Exp Bot. 61:3647–3662.
  • Voznesenskaya EV, Koteyeva NK, Edwards GE, Ocampo G. 2017. Unique photosynthetic phenotypes in Portulaca (Portulacaceae): c 3-C4 intermediates and NAD-ME C4 species with Pilosoid-type Kranz anatomy. J Exp Bot. 68(2):225–239. doi: 10.1093/jxb/erw393.
  • Walker RP, Paoletti A, Leegood RC, Famiani F. 2016. Phosphorylation of phosphoenolpyruvate carboxykinase (PEPCK) and phosphoenolpyruvate carboxylase (PEPC) in the flesh of fruits. Plant Physiol Biochem. 108:323–327. doi: 10.1016/j.plaphy.2016.07.021.
  • Walter H, Box EO. 1983. Middle east deserts. Ecosystem world. Vol 5. In: West NE, editor. Temperate deserts and semi-deserts. Amsterdam (the Netherlands): Elsevier; p. 79–104.
  • Wang Y, Bräutigam A, Weber AP, Zhu XG. 2014. Three distinct biochemical subtypes of C4 photosynthesis? A modelling analysis. J Exp Bot. 65(13):3567–3578. doi: 10.1093/jxb/eru058.
  • Weissmann S, Ma F, Furuyama K, Gierse J, Berg H, Shao Y, Taniguchi M, Allen DK, Brutnell TP. 2016. Interactions of C4 subtype metabolic activities and transport in maize are revealed through the characterization of DCT2 mutants. Plant Cell. 28(2):466–484. doi: 10.1105/tpc.15.00497.
  • Wingler A, Walker RP, Chen Z-H, Leegood RC. 1999. Phosphoenolpyruvate carboxykinase is involved in the decarboxylation of aspartate in the bundle sheath of maize. Plant Physiol. 120(2):539–546. doi: 10.1104/pp.120.2.539.
  • Winter K. 1981. C4 plants of high biomass in arid regions of Asia - occurrence of C4 photosynthesis in Chenopodiaceae and Polygonaceae from the Middle East and USSR. Oecologia. 48(1):100–106. doi: 10.1007/BF00346994.
  • Winter K, Kramer D, Troughton JH, Card KA, Fischer K. 1977. C4 pathway of photosynthesis in a member of the Polygonaceae: Calligonum persicum (Boiss. & Buhse) Boiss. Z Pflanzenphysiol. 81:341–346.
  • Wintermans JFGM, De Mots A. 1965. Spectrophotometric characteristics of chlorophylls a and b and their phenophytins in ethanol. Biochim Biophys Acta. 109:448–453.
  • Yoshimura Y, Kubota F, Ueno O. 2004. Structural and biochemical bases of photorespiration in C4 plants: quantification of organelles and glycine decarboxylase. Planta. 220(2):307–317. doi: 10.1007/s00425-004-1335-1.
  • Young SNR, Sack L, Sporck-Koehler MJ, Lundgren MR. 2020. Why is C4 photosynthesis so rare in trees? J Exp Bot. 71(16):4629–4638. doi: 10.1093/jxb/eraa234.
  • Zohary M. 1972. Flora Palaestina, part 2—text, Platanaceae to Umbelliferae. Jerusalem (Israel): The Israel Academy of Science and Humanities.

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