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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Diversity in structure and forms of carbon assimilation in photosynthetic organs in Cleome (Cleomaceae)

Elena V. Voznesenskaya A , Nuria K. Koteyeva A , Asaph Cousins B and Gerald E. Edwards B C
+ Author Affiliations
- Author Affiliations

A Laboratory of Anatomy and Morphology, Komarov Botanical Institute of the Russian Academy of Sciences, St Petersburg, Russia.

B School of Biological Sciences, Washington State University, Pullman, WA 99164-4236, USA.

C Corresponding author. Email: edwardsg@wsu.edu

Functional Plant Biology 45(10) 983-999 https://doi.org/10.1071/FP17323
Submitted: 17 November 2017  Accepted: 23 March 2018   Published: 26 April 2018

Abstract

Photosynthesis in different organs of Cleome was analysed in four species known to have differences in leaf photosynthesis: Cleome africana Botsch. (C3), Cleome paradoxa R.Br. (C3-C4 intermediate), Cleome angustifolia Forssk. and Cleome gynandra L. (C4). The chlorophyll content, carbon isotope composition, stomatal densities, anatomy, levels and compartmentation of some key photosynthetic enzymes, and the form and function of photosynthesis were determined in different organs of these species. In the three xerophytes, C. africana, C. paradoxa, and C. angustifolia, multiple organs contribute to photosynthesis (cotyledons, leaves, petioles, stems and pods) which is considered important for their survival under arid conditions. In C. africana, all photosynthetic organs have C3 photosynthesis. In C. paradoxa, cotyledons, leaves, stems and petioles have C3-C4 type features. In C. angustifolia, the pods have C3 photosynthesis, whereas all other organs have C4 photosynthesis with Kranz anatomy formed by a continuous, dual layer of chlorenchyma cells. In the subtropical C4 species C. gynandra, cotyledons, leaves, and pods develop C4 photosynthesis, with Kranz anatomy around individual veins; but not in stems and petioles which have limited function of photosynthesis. The diversity in forms and the capacity of photosynthesis in organs of these species to contribute to their carbon economy is discussed.

Additional keywords: chlorenchyma, chloroplast ultrastructure, Cleome, Cleomaceae, C3 plants, C4 plants, immunolocalisation, Kranz anatomy, petiole, stem and pod anatomy, photosynthetic enzymes.


References

Andrews AK, Svec LV (1975) Photosynthetic activity of soybean pods at different growth stages compared to leaves. Canadian Journal of Plant Science 55, 501–505.
Photosynthetic activity of soybean pods at different growth stages compared to leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2MXkt1GhsrY%3D&md5=a1c8f143d85a155c9a64f647c8463180CAS |

Aschan G, Pfanz H (2003) Non-foliar photosynthesis – a strategy of additional carbon acquisition. Flora – Morphology, Distribution, Functional Ecology of Plants 198, 81–97.
Non-foliar photosynthesis – a strategy of additional carbon acquisition.Crossref | GoogleScholarGoogle Scholar |

Atkins CA, Kuo J, Pate JS (1977) Photosynthetic pod wall of pea (Pisum sativum L.). Plant Physiology 60, 779–786.
Photosynthetic pod wall of pea (Pisum sativum L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1cXjsVKrtQ%3D%3D&md5=1651d24aaafc3471bed8d7651ef46f90CAS |

Batanouny KH, Baeshin NA (1983) Plant communities along the Medina-Badr road across the Hejaz mountains, Saudi Arabia. Vegetatio 53, 33–43.
Plant communities along the Medina-Badr road across the Hejaz mountains, Saudi Arabia.Crossref | GoogleScholarGoogle Scholar |

Behboudian MH, Ma Q, Turner NC, Palta JA (2000) Discrimination against 13CO2 in leaves, pod walls, and seeds of water-stressed chickpea. Photosynthetica 38, 155–157.
Discrimination against 13CO2 in leaves, pod walls, and seeds of water-stressed chickpea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmsFSrtbg%3D&md5=bbadc77d3a3a7300a5ccbbf8d24f05d3CAS |

Bender MM (1971) Variations in the 13C/12C ratios of plants in relation to the pathway of photosynthetic carbon dioxide fixation. Phytochemistry 10, 1239–1244.
Variations in the 13C/12C ratios of plants in relation to the pathway of photosynthetic carbon dioxide fixation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3MXkvVGgu7Y%3D&md5=bec16ce51262c8b10173ffaa44a97bc1CAS |

Bennett EJ, Roberts JA, Wagstaff C (2011) The role of the pod in seed development: strategies for manipulating yield. New Phytologist 190, 838–853.
The role of the pod in seed development: strategies for manipulating yield.Crossref | GoogleScholarGoogle Scholar |

Bossard CC, Rejmanek M (1992) Why have green stems? Functional Ecology 6, 197–205.
Why have green stems?Crossref | GoogleScholarGoogle Scholar |

Boyd CN, Franceschi VR, Chuong SDX, Akhani H, Kiirats O, Smith M, Edwards GE (2007) Flowers of Bienertia cycloptera and Suaeda aralocaspica (Chenopodiaceae) complete the life cycle performing single-cell C4 photosynthesis. Functional Plant Biology 34, 268–281.
Flowers of Bienertia cycloptera and Suaeda aralocaspica (Chenopodiaceae) complete the life cycle performing single-cell C4 photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXksFOlurs%3D&md5=8a8c186b6873cbd79c284b50b4f74075CAS |

Brown WV (1975) Variations in anatomy, associations, and origin of Kranz tissue. American Journal of Botany 62, 395–402.
Variations in anatomy, associations, and origin of Kranz tissue.Crossref | GoogleScholarGoogle Scholar |

Brown NJ, Palmer BG, Stanley S, Hajaji H, Janacek SH, Astley HM, Parsley K, Kajala K, Quick WP, Trenkamp S, Fernie AR, Maurino VG, Hibberd JM (2010) C4 acid decarboxylases required for C4 photosynthesis are active in the mid-vein of the C3 species Arabidopsis thaliana, and are important in sugar and amino acid metabolism. The Plant Journal 61, 122–133.
C4 acid decarboxylases required for C4 photosynthesis are active in the mid-vein of the C3 species Arabidopsis thaliana, and are important in sugar and amino acid metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXovF2ksw%3D%3D&md5=f760b812830d168cf31ae4fd4ba7d252CAS |

Carolin RC, Jacobs SWL, Vesk M (1975) Leaf structure in Chenopodiaceae. Botanische Jahrbücher für Systematik, Pflanzengeschichte und Pflanzengeographie 95, 226–255.

Carolin RC, Jacobs SWL, Vesk M (1978) Kranz cells and mesophyll in the Chenopodiales. Australian Journal of Botany 26, 683–698.
Kranz cells and mesophyll in the Chenopodiales.Crossref | GoogleScholarGoogle Scholar |

Comstock JP, Ehleringer JR (1988) Contrasting photosynthetic behavior in leaves and twigs of Hymenoclea salsola, a green-twigged warm desert shrub. American Journal of Botany 75, 1360–1370.
Contrasting photosynthetic behavior in leaves and twigs of Hymenoclea salsola, a green-twigged warm desert shrub.Crossref | GoogleScholarGoogle Scholar |

Dengler NG, Nelson T (1999) Leaf structure and development in C4 plants. In ‘C4 plant biology. Physiological ecology series’. (Eds RF Sage, RK Monson) pp. 133–172. (Academic Press: San Diego, CA, USA)

Edwards GE, Ku MSB (1987) The biochemistry of C3-C4 intermediates. In ‘The biochemistry of plants. Vol. 10. Photosynthesis’. (Eds MD Hatch, NK Boardman) pp. 275–325. (Academic Press, Inc.: New York)

Edwards GE, Voznesenskaya EV (2011) C4 photosynthesis: Kranz forms and single-cell C4 in terrestrial plants. In ‘C4 photosynthesis and related CO2 concentrating mechanisms. Vol. 32’. (Eds AS Raghavendra, RF Sage) pp. 29–61. (Springer: Dordrecht, The Netherlands)

Edwards GE, Walker DA (1983) ‘C3, C4: mechanisms, and cellular and environmental regulation, of photosynthesis’. (Blackwell Scientific Publications: Oxford, UK)

Eggli U (2002) ‘Illustrated handbook of succulent plants: dicotyledons.’ (Springer: Berlin)

Ehleringer JR, Comstock JP, Cooper TA (1987) Leaf-twig carbon isotope ratio differences in photosynthetic-twig desert shrubs. Oecologia 71, 318–320.
Leaf-twig carbon isotope ratio differences in photosynthetic-twig desert shrubs.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC1czotVOksw%3D%3D&md5=debdf7f044c3019120d224603a03060eCAS |

Elffers J, Graham RA, Dewolf GP (1964) Capparidaceae. In ‘Flora of tropical east Africa’. (Eds CE Hubbard, E Milne-Redhead) pp. 1–88. (Whitefriars Press Ltd: London)

Fahn A, Cutler DF (1992) ‘Xerophytes.’ (Gebruder Borntraeger: Berlin, Stuttgart)

Feodorova TA, Voznesenskaya EV, Edwards GE, Roalson EH (2010) Biogeographic patterns of diversification and the origins of C4 in Cleome (Cleomaceae). Systematic Botany 35, 811–826.
Biogeographic patterns of diversification and the origins of C4 in Cleome (Cleomaceae).Crossref | GoogleScholarGoogle Scholar |

Flinn A, Atkins C, Pate J (1977) Significance of photosynthetic and respiratory exchanges in the carbon economy of the developing pea fruit. Plant Physiology 60, 412–418.
Significance of photosynthetic and respiratory exchanges in the carbon economy of the developing pea fruit.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cnht1artg%3D%3D&md5=bab148038fb417ce9f17ac0cc0b9225fCAS |

Friis I, Vollesen K (1998) ‘Flora of the Sudan-Uganda border area east of the Nile.’ (Kongelige Danske videnskabernes selskab: Kommissionær, Munksgaard: Copenhagen)

Furbank RT, White R, Palta JA, Turner NC (2004) Internal recycling of respiratory CO2 in pods of chickpea (Cicer arietinum L.): the role of pod wall, seed coat, and embryo. Journal of Experimental Botany 55, 1687–1696.
Internal recycling of respiratory CO2 in pods of chickpea (Cicer arietinum L.): the role of pod wall, seed coat, and embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXntValtrc%3D&md5=cace2b96ec2e28d4d73dbf791cd9951cCAS |

Ghashghaie J, Badeck F, Lanigan G, Nogués S, Tcherkez G, Deléens E, Cornic G, Griffiths H (2003) Carbon isotope discrimination during dark respiration and photorespiration in C3 plants. Phytochemistry Reviews 2, 145–161.
Carbon isotope discrimination during dark respiration and photorespiration in C3 plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXptlyitw%3D%3D&md5=acb5aeaddaf4d5f847612f0ba34bf06aCAS |

Ghashghaie J, Badeck F, Girardin C, Sketriené D, Lamothe-Sibold M, Werner R (2015) Changes in δ13C of respired CO2 and organic matter of different organs during early ontogeny in peanut plants. Isotopes in Environmental and Health Studies 51, 93–108.
Changes in δ13C of respired CO2 and organic matter of different organs during early ontogeny in peanut plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXjsFWntr8%3D&md5=3d6c22dbdb5c38750c0786f0075f2289CAS |

Gibson AC (1998) Photosynthetic organs of desert plants. Bioscience 48, 911–920.
Photosynthetic organs of desert plants.Crossref | GoogleScholarGoogle Scholar |

Hatch MD (1987) C4 photosynthesis: a unique blend of modified biochemistry, anatomy and ultrastructure. Biochimica et Biophysica Acta 895, 81–106.
C4 photosynthesis: a unique blend of modified biochemistry, anatomy and ultrastructure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXjs1Oisw%3D%3D&md5=3c8f1c9be542fd52610c76ff6ea1ff5bCAS |

Hibberd JH, Quick P (2002) Characteristics of C4 photosynthesis in stems and petioles of C3 flowering plants. Nature 415, 451–454.
Characteristics of C4 photosynthesis in stems and petioles of C3 flowering plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtVKjsro%3D&md5=ea7dda5408b18c286e14ce65bcd338cdCAS |

Hooker JD (1875) ‘Flora of British India.’ (L Reeve & Co. Ltd: London)

Iltis HH (1960) Studies in the Capparidaceae. VII. Old World Cleomes adventive in the New World. Brittonia 12, 279–294.
Studies in the Capparidaceae. VII. Old World Cleomes adventive in the New World.Crossref | GoogleScholarGoogle Scholar |

Johnson H (1975) Gas-exchange strategies in desert plants. In ‘Perspectives in biophysical ecology’. (Eds D Gates, R Schmerl) pp. 105–120. (Springer-Verlag: New York)

Kamel WM, Abd El-Ghani MM, El-Bouce MM (2010) Cleomaceae as a distinct family in the flora of Egypt. African Journal of Plant Science and Biotechnology 4, 11–16.

Kanai R, Edwards G (1999) The biochemistry of C4 photosynthesis. In ‘C4 plant biology. physiological ecology series’. (Eds RF Sage, RK Monson) pp. 49–87. (Academic Press: San Diego, CA, USA)

Koteyeva NK, Voznesenskaya EV, Edwards GE (2011) Diversity in forms of C4 in genus Cleome (Cleomaceae). Annals of Botany 107, 269–283.
Diversity in forms of C4 in genus Cleome (Cleomaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlansrg%3D&md5=645719a2db2a16d6ed713992265f24f1CAS |

Koteyeva NK, Voznesenskaya EV, Cousins A, Edwards GE (2014) Differentiation of C4 photosynthesis along a leaf developmental gradient in two Cleome species having different forms of Kranz anatomy. Journal of Experimental Botany 65, 3525–3541.
Differentiation of C4 photosynthesis along a leaf developmental gradient in two Cleome species having different forms of Kranz anatomy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtFCrurjF&md5=5ab1494838d0918023754d4d14bd4513CAS |

Kürschner H (1998) Biogeography and introduction to vegetation. In ‘Vegetation of Arabian peninsula’. (Eds SA Ghazanfar, M Fisher) pp. 63–98. (Springer Science + Business Media: Berlin)

Lauterbach M, Billakurthi K, Kadereit G, Ludwig M, Westhoff P, Gowik U (2017) C3 cotyledons are followed by C4 leaves: intra-individual transcriptome analysis of Salsola soda (Chenopodiaceae). Journal of Experimental Botany 68, 161–176.
C3 cotyledons are followed by C4 leaves: intra-individual transcriptome analysis of Salsola soda (Chenopodiaceae).Crossref | GoogleScholarGoogle Scholar |

Liu H-m, Li Y, Bu G-j, Lv W, Cui L, Cang J, Wang X-d (2008) Effects of photosynthate transportation and distribution in soybean pods on the development of soybean seeds. Journal of Nuclear Agricultural Sciences 22, 519–523.

Long JJ, Berry JO (1996) Tissue-specific and light-mediated expression of the C4 photosynthetic NAD-dependent malic enzyme of amaranth mitochondria. Plant Physiology 112, 473–482.
Tissue-specific and light-mediated expression of the C4 photosynthetic NAD-dependent malic enzyme of amaranth mitochondria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XmsFKlsr0%3D&md5=af68f1d4d2c9ee8e96b1449b2217be08CAS |

Ma Q, Behboudian MH, Turner NC, Palta JA (2001) Gas exchange by pods and subtending leaves and internal recycling of CO2 by pods of chickpea (Cicer arietinum L.) subjected to water deficits. Journal of Experimental Botany 52, 123–131.

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. The Plant Journal 51, 886–896.
Cleome, a genus closely related to Arabidopsis, contains species spanning a developmental progression from C3 to C4 photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVKmurfJ&md5=21ea824943a88b6a7f47d966ddb770bcCAS |

Maxwell K, Badger MR, Osmond CB (1998) A comparison of CO2 and O2 exchange patterns and the relationship with chlorophyll fluorescence during photosynthesis in C3 and CAM plants. Functional Plant Biology 25, 45–52.

Muhaidat R, Sage RF, Dengler NG (2007) Diversity of Kranz anatomy and biochemistry in C4 eudicots. American Journal of Botany 94, 362–381.
Diversity of Kranz anatomy and biochemistry in C4 eudicots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXktFOjsb8%3D&md5=c28cf92a93884eb6873b07f91af1ccb7CAS |

Norton J, Abdul Majid S, Allan D, Al Safran M, Böer B, Richer R (2009) ‘An illustrated checklist of the flora of Qatar.’ (Ashford Colour Press Ltd: Gosport, UK)

Oliver D (1868) ‘Flora of tropical Africa.’ (L. Reeve & Co.: London)

Pyankov VI, Kuzmin AN, Demidov ED, Maslov AI (1992) Diversity of biochemical pathways of CO2 fixation in plants of the families Poaceae and Chenopodiaceae from the arid zone of Central Asia. Soviet Plant Physiology 39, 411–420.

Peter G, Katinas L (2003) A new type of Kranz anatomy in Asteraceae. Australian Journal of Botany 51, 217–226.
A new type of Kranz anatomy in Asteraceae.Crossref | GoogleScholarGoogle Scholar |

Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of the chlorophyll standards by atomic absorption spectroscopy. Biochimica et Biophysica Acta 975, 384–394.
Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of the chlorophyll standards by atomic absorption spectroscopy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXkvFehtL4%3D&md5=14f84141eddcb544e9e58c981c910743CAS |

Post GE (1896) ‘Flora of Syria, Palestine and Sinai; from the Taurus to Ras Muhammad, and from the Mediterranean Sea to the Syrian desert.’ (Sirian Protestant College: Beirut, Siria)

Pyankov VI, Artyusheva EG, Edwards G (1999a) Formation of C4 syndrome in leaves and cotyledons of Kochia scoparia and Salsola collina (Chenopodiaceae). Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 46, 452–466.

Pyankov VI, Black CC, Artyusheva EG, Voznesenskaya EV, Ku MSB, Edwards GE (1999b) Features of photosynthesis in Haloxylon species of Chenopodiaceae that are dominant plants in Central Asian deserts. Plant & Cell Physiology 40, 125–134.
Features of photosynthesis in Haloxylon species of Chenopodiaceae that are dominant plants in Central Asian deserts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXktVOhsQ%3D%3D&md5=07f0494841d1dc556a7e32bbf9fd50f2CAS |

Pyankov VI, Voznesenskaya EV, Kuzmin AN, Ku MSB, Ganko E, Franceschi VR, Black CC, Edwards GE (2000) Occurrence of C3 and C4 photosynthesis in cotyledons and leaves of Salsola species (Chenopodiaceae). Photosynthesis Research 63, 69–84.
Occurrence of C3 and C4 photosynthesis in cotyledons and leaves of Salsola species (Chenopodiaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlsVymtbo%3D&md5=1a7cf0882f47de8dae891b40393aacc0CAS |

Rawsthorne S, Hylton CM, Smith AM, Woolhouse HW (1988) Photorespiratory metabolism and immunogold localization of photorespiratory enzymes in leaves of C3 and C3-C4 intermediate species of Moricandia. Planta 173, 298–308.
Photorespiratory metabolism and immunogold localization of photorespiratory enzymes in leaves of C3 and C3-C4 intermediate species of Moricandia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXhs1CrsLk%3D&md5=94e2a81b21b850ab0bcd28ecf0ed2f0eCAS |

Ruuska SA, Badger MR, Andrews TJ, von Caemmerer S (2000) Photosynthetic electron sinks in transgenic tobacco with reduced amounts of Rubisco: little evidence for significant Mehler reaction. Journal of Experimental Botany 51, 357–368.
Photosynthetic electron sinks in transgenic tobacco with reduced amounts of Rubisco: little evidence for significant Mehler reaction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhsVKqu7w%3D&md5=e95815b2726f8befa75839d7a12f0393CAS |

Rylott EL, Metzlaff K, Rawsthorne S (1998) Developmental and environmental effects on the expression of the C3-C4 intermediate phenotype in Moricandia arvensis. Plant Physiology 118, 1277–1284.
Developmental and environmental effects on the expression of the C3-C4 intermediate phenotype in Moricandia arvensis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhtFU%3D&md5=81fe8de5be50eaf82ab8ce8077a6a58dCAS |

Sage RF (2004) The evolution of C4 photosynthesis. New Phytologist 161, 341–370.
The evolution of C4 photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhsVymuro%3D&md5=41994fe9b2d313e79a8dd5e786dd9b2fCAS |

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). Journal of Experimental Botany 68, 207–223.
Molecular phylogeny and forms of photosynthesis in tribe Salsoleae (Chenopodiaceae).Crossref | GoogleScholarGoogle Scholar |

Setia RC, Setia N, Malik CP (1987) The podwall structure and function in relation to seed development in some legumes. Phyton 27, 205–220.

Sheoran I, Singal H, Singh R (1987) Photosynthetic characteristics of chickpea (Cicer arietinum L.) pod wall during seed development. Indian Journal of Experimental Biology 25, 843–847.

Smith S, Monson R, Anderson J (1997) ‘Physiological ecology of North American desert plants.’ (Springer: Berlin)

Takhtajan A (2009) ‘Flowering plants’. (Springer Science + Business Media: Berlin)

Valladares F (2003) Light heterogeneity in plants: from ecophysiology to species coexistence and biodiversity. In ‘Progress in botany. Vol. 64’. (Eds K Esser, U Lüttge, W Beyschlag, F Hellwig) pp. 439–453. (Springer-Verlag: Berlin)

Vesey-Fitzgerald DF (1957) The vegetation of the Red Sea coast north of Jedda, Saudi Arabia. Journal of Ecology 45, 547–562.
The vegetation of the Red Sea coast north of Jedda, Saudi Arabia.Crossref | GoogleScholarGoogle Scholar |

von Caemmerer S, Ghannoum O, Pengelly J, Cousins A (2014) Carbon isotope discrimination as a tool to explore C4 photosynthesis. Journal of Experimental Botany 65, 3459–3470.
Carbon isotope discrimination as a tool to explore C4 photosynthesis.Crossref | GoogleScholarGoogle Scholar |

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). Journal of Experimental Botany 50, 1779–1795.
Anatomy, chloroplast structure and compartmentation of enzymes relative to photosynthetic mechanisms in leaves and cotyledons of species in the tribe Salsoleae (Chenopodiaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXntFOntw%3D%3D&md5=90ce1418fcd98e55ab9f787102f2f31bCAS |

Voznesenskaya EV, Franceschi VR, Edwards GE (2004) Light-dependent development of single cell C4 photosynthesis in cotyledons of Borszczowia aralocaspica (Chenopodiaceae) during transformation from a storage to a photosynthetic organ. Annals of Botany 93, 177–187.
Light-dependent development of single cell C4 photosynthesis in cotyledons of Borszczowia aralocaspica (Chenopodiaceae) during transformation from a storage to a photosynthetic organ.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXitVKgu74%3D&md5=982fe7ae93d8ef31a0b0815cc997440fCAS |

Voznesenskaya E, Koteyeva NK, Chuong SDX, Ivanova AN, Barroca J, Craven L, Edwards GE (2007) Physiological, anatomical and biochemical characterization of the type of photosynthesis in Cleome species (Cleomaceae). Functional Plant Biology 34, 247–267.
Physiological, anatomical and biochemical characterization of the type of photosynthesis in Cleome species (Cleomaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXksFOlurg%3D&md5=4096031fc7ca272d0270fc9477608cdbCAS |

Voznesenskaya EV, Akhani H, Koteyeva NK, Chuong SDX, Roalson EH, Kiirats O, Franceschi VR, Edwards GE (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, 1715–1734.
Structural, biochemical and physiological characterization of photosynthesis in two C4 subspecies of Tecticornia indica and the C3 species Tecticornia pergranulata (Chenopodiaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmtleltLw%3D&md5=80fd09cd5fbc060e39a6600ecf2237e8CAS |

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). Journal of Experimental Botany 61, 3647–3662.
Revealing diversity in structural and biochemical forms of C4 photosynthesis and a C3-C4 intermediate in genus Portulaca L. (Portulacaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVert7vE&md5=02571f331be843f9b8ac84f2fa554ea7CAS |

Voznesenskaya EV, Koteyeva NK, Akhani H, Roalson EH, Edwards GE (2013) Structural and physiological analyses in Salsoleae (Chenopodiaceae) indicate multiple transitions among C3, intermediate and C4 photosynthesis. Journal of Experimental Botany 64, 3583–3604.
Structural and physiological analyses in Salsoleae (Chenopodiaceae) indicate multiple transitions among C3, intermediate and C4 photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1yrsr3P&md5=dfd50bad6e93574e6ef4f2e5ffab0edaCAS |

Voznesenskaya EV, Koteeva NK, Edwards GE, Ocampo G (2017) Unique photosynthetic phenotypes in Portulaca (Portulacaceae): C3-C4 intermediates and NAD-ME C4 species with Pilosoid-type Kranz anatomy. Journal of Experimental Botany 68, 225–239.
Unique photosynthetic phenotypes in Portulaca (Portulacaceae): C3-C4 intermediates and NAD-ME C4 species with Pilosoid-type Kranz anatomy.Crossref | GoogleScholarGoogle Scholar |

Wahid A, Rasul E (2005) Photosynthesis in leaf, stem, flower, and fruit. In ‘Handbook of photosynthesis’. (Ed. M Pessaraki) pp. 479–497. (CRC Press: Boca Raton, FL, USA)

Wang HL, Grusak MA (2005) Structure and development of Medicago truncatula pod wall and seed coat. Annals of Botany 95, 737–747.
Structure and development of Medicago truncatula pod wall and seed coat.Crossref | GoogleScholarGoogle Scholar |

Wang H, Hou L, Wang M, Mao P (2016) Contribution of the pod wall to seed grain filling in alfalfa. Scientific Reports 6, 26586
Contribution of the pod wall to seed grain filling in alfalfa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XosVSlsro%3D&md5=b83580ca76c79b0469248ce7254d388cCAS |

Zalenski W (1902) Uber die Ausbildung der Nervation bei verschiedenen Pflanzen. Berichte der Deutsche Botanical Geselschaft 20, 433–440.