Significance of C4 Leaf Structure at the Tissue and Cellular Levels

Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 44)


The CO2 concentrating mechanism (CCM) in C4 plants requires a complex coordination of both leaf anatomical and biochemical traits. While there are key traits common across the 60 plus C4 lineages, there is also significant structural and biochemical variation. Traditionally, C4 plants are described as one of three biochemical subtypes based on the primary enzyme used for C4 acid decarboxylation: NADP-malic enzyme (NADP-ME), NAD-malic enzyme (NAD-ME), and phosphoenolpyruvate carboxykinase (PCK). However, there may be biochemical flexibility and overlap between these subtypes. C4 plants typically rely on Kranz-type anatomy that partitions the C4 cycle into the mesophyll (M) cells and the majority of C3 cycle into the bundle-sheath (BS) cells. However, within the succulent Chenopods some NAD-ME type C4 plants use one of two single-cell arrangements to partition and compartmentalize the C4 and C3 cycles. Here we discuss key leaf anatomical traits at the tissue, cellular, and sub-cellular level that influence the efficiency and effectiveness of C4 photosynthesis. Specifically, we discuss preconditioning of leaf traits that increase the evolvability of C4 photosynthesis, the evolutionary transition of organelles from C3 to a C4 leaf, gas and metabolite movement within the leaf, the positioning and maintenance of organelles in M and BS cells, and the movement of M chloroplasts.


Leaf Anatomical Traits NADP-malic Enzyme Kranz-type Anatomy Metabolite Movement Suberized Lamella 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



abscisic acid


net rate of CO2 assimilation




plants using a photorespiratory glycine shuttle to concentrate CO2


plants without a CO2 concentrating mechanism


plants using a 4-carbon CO2 concentrating mechanism


carbonic anhydrase


CO2 partial in the atmosphere


crassulacean acid metabolism


CO2 concentrating mechanism


CO2 partial pressure in the intercellular air space


carbon dioxide


the carbon isotope composition


carbon isotope discrimination




boundary layer conductance


conductance of CO2 between the BS and M cells or the corresponding cellular compartments in the single-cell C4 system


glycine decarboxylase complex


internal conductance of CO2 from the inter-cellular airspace to the initial site of carboxylation


stomatal conductance to either CO2 or H2O




inter-veinal distances


total leaf water conductance


Michaelis-Menten constant of PEPC for HCO3-






million years


NADP-malic enzyme


NAD-malic enzyme






phosphoenolpyruvate carboxykinase






phosphoenolpyruvate carboxylase




the BS surface area per unit leaf area


M surface area exposed to the inter-cellular air space


vascular bundle


in vitro maximum PEPC activity



The research of ABC was supported by the Office of Biological and Environmental Research in the DOE Office of Science (DE-SC0008769) and MT was supported by JSPS KAKENHI Grant Numbers JP26292011 and JP16K14835.


  1. Araus JL, Brown RH, Bouton JH, Serret MD (1990) Leaf anatomical characteristics in Flaveria trinervia (C4), Flaveria brownii (C4-like) and their F1 hybrid. Photosynth Res 26:49–57PubMedGoogle Scholar
  2. Barbour MM, Evans JR, Simonin KA, von Caemmerer S (2016) Online CO2 and H2O oxygen isotope fractionation allows estimation of mesophyll conductance in C4 plants, and reveals that mesophyll conductance decreases as leaves age in both C4 and C3 plants. New Phytol 210:875–889PubMedCrossRefGoogle Scholar
  3. Bellasio C, Lundgren MR (2016) Anatomical constraints to C4 evolution: light harvesting capacity in the bundle sheath. New Phytol 212:485–496PubMedCrossRefGoogle Scholar
  4. Betti M, Bauwe H, Busch FA, Fernie AR, Keech O, Levey M et al (2016) Manipulating photorespiration to increase plant productivity: recent advances and perspectives for crop improvement. J Exp Bot 67:2977–2988PubMedCrossRefGoogle Scholar
  5. Brodribb TJ, Feild TS (2010) Leaf hydraulic evolution led a surge in leaf photosynthetic capacity during early angiosperm diversification. Ecol Lett 13:175–183PubMedCrossRefGoogle Scholar
  6. Brown RH, Hattersley PW (1989) Leaf anatomy of C3-C4 species as related to evolution of C4 photosynthesis. Plant Physiol 91:1543–1550PubMedPubMedCentralCrossRefGoogle Scholar
  7. Busch FA, Sage TL, Cousins AB, Sage RF (2013) C3 plants enhance rates of photosynthesis by reassimilating photorespired and respired CO2. Plant Cell Environ 36:200–212PubMedCrossRefGoogle Scholar
  8. Cheng SH, Moore BD, Edwards GE, Ku MSB (1988) Photosynthesis in Flaveria brownii, a C4-like species: leaf anatomy, characteristics of CO2 exchange, compartmentation of photosynthetic enzymes, and metabolism of 14CO2. Plant Physiol 87:867–873PubMedPubMedCentralCrossRefGoogle Scholar
  9. Christin PA, Osborne CP, Chatelet DS, Columbus JT, Besnard G, Hodkinson TR et al (2013) Anatomical enablers and the evolution of C4 photosynthesis in grasses. Proc Natl Acad Sci U S A 110:1381–1386PubMedCrossRefGoogle Scholar
  10. Chuong SDX, Franceschi VR, Edwards GE (2006) The cytoskeleton maintains organelle partitioning required for single-cell C4 photosynthesis in Chenopodiaceae species. Plant Cell 18:2207–2223PubMedPubMedCentralCrossRefGoogle Scholar
  11. Cousins AB, Badger MR, von Caemmerer S (2006) Carbonic anhydrase and its influence on carbon isotope discrimination during C4 photosynthesis. Insights from antisense RNA in Flaveria bidentis. Plant Physiol 141:232–242PubMedPubMedCentralCrossRefGoogle Scholar
  12. Cousins AB, Baroli I, Badger MR, Ivakov A, Lea PJ, Leegood RC, von Caemmerer S (2007) The role of phosphoenolpyruvate carboxylase during C4 photosynthetic isotope exchange and stomatal conductance. Plant Physiol 145:1006–1017PubMedPubMedCentralCrossRefGoogle Scholar
  13. Covshoff S, Hibberd JM (2012) Integrating C4 photosynthesis into C3 crops to increase yield potential. Curr Opin Biotechnol 23:209–214PubMedCrossRefGoogle Scholar
  14. D’Andrea RM, Andreo CS, Lara MV (2014) Deciphering the mechanisms involved in Portulaca oleracea (C4) response to drought: metabolic changes including crassulacean acid-like metabolism induction and reversal upon re-watering. Physiol Plant 152:414–430PubMedCrossRefGoogle Scholar
  15. 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 28:1461–1471PubMedPubMedCentralCrossRefGoogle Scholar
  16. DeBlasio SL, Luesse DL, Hangarter RP (2005) A plant-specific protein essential for blue-light-induced chloroplast movements. Plant Physiol 139:101–114PubMedPubMedCentralCrossRefGoogle Scholar
  17. Dengler NG, Nelson T (1999) Leaf structure and development in C4 plants. In: Sage RF, Monson RK (eds) C4 plant biology. Academic, San Diego, pp 133–172CrossRefGoogle Scholar
  18. Dengler NG, Dengler RE, Hattersley PW (1986) Comparative bundle sheath and mesophyll differentiation in the leaves of the C4 grasses Panicum effusum and P. bulbosum. Am J Bot 73:1431–1442CrossRefGoogle Scholar
  19. Dengler NG, Dengler RE, Donelly PM, Hattersley PW (1994) Quantitative leaf anatomy of C3 and C4 grasses (Poaceae): bundle sheath and mesophyll surface area relationships. Ann Bot 73:241–255CrossRefGoogle Scholar
  20. Eastman PAK, Dengler NG, Peterson CA (1988) Suberized bundle sheaths in grasses (Poaceae) of different photosynthetic types. I. Anatomy, ultrastructure and histochemistry. Protoplasma 142:92–111CrossRefGoogle Scholar
  21. Edwards EJ (2014) The inevitability of C4 photosynthesis. elife 3:e03702PubMedPubMedCentralCrossRefGoogle Scholar
  22. Edwards GE, Voznesenskaya EV (2011) C4 photosyntehsis: Kranz forms and single-cell C4 in terrestrial plants. In: Raghavendra AS, Sage RF (eds) C4 photosynthesis and related CO2 concentrating mechanisms. Advances in photosynthesis and respiration, vol 32. Springer, Dordrecht, pp 29–61CrossRefGoogle Scholar
  23. Edwards GE, Furbank RT, Hatch MD, Osmond CB (2001) What does it take to be C4? Lessons from the evolution of C4 photosynthesis. Plant Physiol 125:46–49PubMedPubMedCentralCrossRefGoogle Scholar
  24. Edwards GE, Franceschi VR, Voznesenskaya EV (2004) Single-cell C4 photosynthesis versus the dual-cell (Kranz) paradigm. Annu Rev Plant Biol 55:173–196PubMedCrossRefGoogle Scholar
  25. Edwards EJ, Osborne CP, Stromberg CA, Smith SA, Consortium CG, Bond WJ et al (2010) The origins of C4 grasslands: integrating evolutionary and ecosystem science. Science 328:587–591PubMedPubMedCentralCrossRefGoogle Scholar
  26. Ellsworth PZ, Cousins AB (2016) Carbon isotopes and water use efficiency in C4 plants. Curr Opin Plant Biol 31:155–161PubMedCrossRefGoogle Scholar
  27. Erlinghaeuser M, Hagenau L, Wimmer D, Offermann S (2016) Development, subcellular positioning and selective protein accumulation in the dimorphic chloroplasts of single-cell C4 species. Curr Opin Plant Biol 31:76–82PubMedCrossRefGoogle Scholar
  28. Evans JR, von Caemmerer S (1996) Carbon dioxide diffusion inside leaves. Plant Physiol 110:339–346PubMedPubMedCentralCrossRefGoogle Scholar
  29. Evans JR, von Caemmerer S, Setchell BA, Hudson GS (1994) The relationship between CO2 transfer conductance and leaf anatomy in transgenic tobacco with a reduced content of Rubisco. Aust J Plant Physiol 21:475–495CrossRefGoogle Scholar
  30. Farquhar GD (1983) On the nature of carbon isotope discrimination in C4 species. Aust J Plant Physiol 10:205–226CrossRefGoogle Scholar
  31. Farquhar GD, Cernusak LA (2012) Ternary effects on the gas exchange of isotopologues of carbon dioxide. Plant Cell Environ 35:1221–1231PubMedCrossRefPubMedCentralGoogle Scholar
  32. Fladung M (1994) Genetic variants of Panicum maximum (Jacq.) in C4 photosynthetic traits. J Plant Physiol 143:165–172CrossRefGoogle Scholar
  33. Flexas J, Díaz-Espejo A, Galmés J, Kaldenhoff R, Medrano H, Ribas-Carbó M (2007) Rapid variations of mesophyll conductance in response to changes in CO2 concentration around leaves. Plant Cell Environ 30:1284–1298PubMedCrossRefPubMedCentralGoogle Scholar
  34. Flexas J, Ribas-Carbó M, Diaz-Espejo A, Galmés J, Medrano H (2008) Mesophyll conductance to CO2: current knowledge and future prospects. Plant Cell Environ 31:602–621PubMedCrossRefPubMedCentralGoogle Scholar
  35. Flexas J, Barbour MM, Brendel O, Cabrera HM, Carriqui M, Diax-Espejo A et al (2012) Mesophyll diffusion conductance to CO2: an unappreciated central player in photosynthesis. Plant Sci 193-194:70–84PubMedCrossRefPubMedCentralGoogle Scholar
  36. Flexas J, Scoffoni C, Gago J, Sack L (2013) Leaf mesophyll conductance and leaf hydraulic conductance: an introduction to their measurement and coordination. J Exp Bot 64:3965–3981PubMedCrossRefPubMedCentralGoogle Scholar
  37. Flexas J, Diaz-Espejo A, Conesa MA, Coopman RE, Douthe C, Gago J et al (2016) Mesophyll conductance to CO2 and Rubisco as targets for improving intrinsic water use efficiency in C3 plants. Plant Cell Environ 39:965–982PubMedCrossRefPubMedCentralGoogle Scholar
  38. Fouracre JP, Ando S, Langdale JA (2014) Cracking the Kranz enigma with systems biology. J Exp Bot 65:3327–3339PubMedCrossRefPubMedCentralGoogle Scholar
  39. Furbank RT (2011) Evolution of the C4 photosynthetic mechanism: are there really three C4 acid decarboxylation types? J Exp Bot 62:3103–3108CrossRefGoogle Scholar
  40. Furbank RT, Jenkins CL, Hatch MD (1989) CO2 concentrating mechanism of C4 photosynthesis: permeability of isolated bundle sheath cells to inorganic carbon. Plant Physiol 91:1364–1371PubMedPubMedCentralCrossRefGoogle Scholar
  41. Gillon JS, Yakir D (2000) Naturally low carbonic anhydrase activity in C4 and C3 plants limits discrimination against (COO)-O18 during photosynthesis. Plant Cell Environ 23:903–915CrossRefGoogle Scholar
  42. Griffiths H, Weller G, Toy LF, Dennis RJ (2013) You’re so vein: bundle sheath physiology, phylogeny and evolution in C3 and C4 plants. Plant Cell Environ 36:249–261PubMedCrossRefGoogle Scholar
  43. Guralnick LJ, Edwards G, Ku MSB, Hockema B, Franceschi VR (2002) Photosynthetic and anatomical characteristics in the C4-crassulacean acid metabolism-cycling plant, Portulaca grandiflora. Funct Plant Biol 29:763–773CrossRefGoogle Scholar
  44. Gutierrez M, Gracen VE, Edwards GE (1974) Biochemical and cytological relationships in C4 plants. Planta 119:279–300PubMedCrossRefGoogle Scholar
  45. Hasan R, Ohnuki Y, Kawasaki M, Taniguchi M, Miyake H (2005) Differential sensitivity of chloroplasts in mesophyll and bundle sheath cells in maize, an NADP-malic enzyme-type C4 plant, to salinity stress. Plant Prod Sci 8:567–577CrossRefGoogle Scholar
  46. Hasan R, Kawasaki M, Taniguchi M, Miyake H (2006) Salinity stress induces granal development in bundle sheath chloroplasts of maize, an NADP-malic enzyme-type C4 plant. Plant Prod Sci 9:256–265CrossRefGoogle Scholar
  47. Hassiotou F, Ludwig M, Renton M, Veneklaas EJ, Evans JR (2009) Influence of leaf dry mass per area, CO2, and irradiance on mesophyll conductance in sclerophylls. J Exp Bot 60:2303–2314PubMedCrossRefPubMedCentralGoogle Scholar
  48. Hatakeyama Y, Ueno O (2016) Intracellular position of mitochondria and chloroplasts in bundle sheath and mesophyll cells of C3 grasses in relation to photorespiratory CO2 loss. Plant Prod Sci 19:540–551CrossRefGoogle Scholar
  49. Hatch MD, Kagawa T, Craig S (1975) Subdivision of C4-pathway species based on differing C4 acid decarboxylating systems and ultrastructural features. Aust J Plant Physiol 2:111–128CrossRefGoogle Scholar
  50. Hatch MD, Agostino A, Jenkins CLD (1995) Measurement of the leakage of CO2 from bundle-sheath cells of leaves during C4 photosynthesis. Plant Physiol 108:173–181PubMedPubMedCentralCrossRefGoogle Scholar
  51. Hattersley PW, Browning AJ (1981) Occurrence of the suberized lamella in leaves of grasses of different photosynthetic types. I. In parenchymatous bundle sheaths and PCR ("Kranz") sheaths. Protoplasma 109:371–401CrossRefGoogle Scholar
  52. Heckmann D, Schulze S, Denton A, Gowik U, Westhoff P, Weber AP, Lercher MJ (2013) Predicting C4 photosynthesis evolution: modular, individually adaptive steps on a Mount Fuji fitness landscape. Cell 153:1579–1588PubMedCrossRefGoogle Scholar
  53. Holaday AS, Lee KW, Chollet R (1984) C3-C4 intermediate species in the genus Flaveria: leaf anatomy, ultrastructure, and the effect of O2 on the CO2 compensation concentration. Planta 160:25–32PubMedCrossRefGoogle Scholar
  54. Inoue Y, Shibata K (1974) Comparative examination of terrestrial plant leaves in terms of light-induced absorption changes due to chloroplast rearrangements. Plant Cell Physiol 15:717–721CrossRefGoogle Scholar
  55. Jenkins CL, Furbank RT, Hatch MD (1989a) Inorganic carbon diffusion between C4 mesophyll and bundle sheath cells: direct bundle sheath CO2 assimilation in intact leaves in the presence of an inhibitor of the C4 pathway. Plant Physiol 91:1356–1363PubMedPubMedCentralCrossRefGoogle Scholar
  56. Jenkins CL, Furbank RT, Hatch MD (1989b) Mechanism of C4 photosynthesis: a model describing the inorganic carbon pool in bundle sheath cells. Plant Physiol 91:1372–1381PubMedPubMedCentralCrossRefGoogle Scholar
  57. Kanai R, Edwards GE (1999) The biochemistry of C4 photosynthesis. In: Sage R, Monson R (eds) C4 plant biology. Academic, San Diego, pp 49–87CrossRefGoogle Scholar
  58. Kandasamy MK, Meagher RB (1999) Actin-organelle interaction: association with chloroplast in Arabidopsis leaf mesophyll cells. Cell Motil Cytoskeleton 44:110–118PubMedCrossRefGoogle Scholar
  59. Khoshravesh R, Stinson CR, Stata M, Busch FA, Sage RF, Ludwig M, Sage TL (2016) C3-C4 intermediacy in grasses: organelle enrichment and distribution, glycine decarboxylase expression, and the rise of C2 photosynthesis. J Exp Bot 67:3065–3078PubMedPubMedCentralCrossRefGoogle Scholar
  60. King J, Edwards GE, Cousins AB (2012) The efficiency of the CO2-concentrating mechanism during single-cell C4 photosynthesis. Plant Cell Environ 35:513–523PubMedCrossRefGoogle Scholar
  61. Kinsman EA, Pyke KA (1998) Bundle sheath cells and cell-specific plastid development in Arabidopsis leaves. Development 125:1815–1822PubMedGoogle Scholar
  62. Kobayashi H, Yamada M, Taniguchi M, Kawasaki M, Sugiyama T, Miyake H (2009) Differential positioning of C4 mesophyll and bundle sheath chloroplasts: recovery of chloroplast positioning requires the actomyosin system. Plant Cell Physiol 50:129–140PubMedCrossRefGoogle Scholar
  63. Kondo A, Kaikawa J, Funaguma T, Ueno O (2004) Clumping and dispersal of chloroplasts in succulent plants. Planta 219:500–506PubMedCrossRefGoogle Scholar
  64. Kong SG, Wada M (2014) Recent advances in understanding the molecular mechanism of chloroplast photorelocation movement. Biochim Biophys Acta 1837:522–530PubMedCrossRefGoogle Scholar
  65. Königer M, Bollinger N (2012) Chloroplast movement behavior varies widely among species and does not correlate with high light stress tolerance. Planta 236:411–426PubMedCrossRefGoogle Scholar
  66. Koteyeva NK, Voznesenskaya EV, Berry JO, Cousins AB, Edwards GE (2016) The unique structural and biochemical development of single cell C4 photosynthesis along longitudinal leaf gradients in Bienertia sinuspersici and Suaeda aralocaspica (Chenopodiaceae). J Exp Bot 67:2587–2601PubMedPubMedCentralCrossRefGoogle Scholar
  67. Kromdijk J, Ubierna N, Cousins AB, Griffiths H (2014) Bundle-sheath leakiness in C4 photosynthesis: a careful balancing act between CO2 concentration and assimilation. J Exp Bot 65:3443–3457PubMedCrossRefGoogle Scholar
  68. Ku MSB, Wu JR, Dai ZY, Scott RA, Chu C, Edwards GE (1991) Photosynthetic and photorespiratory characteristics of Flaveria species. Plant Physiol 96:518–528PubMedPubMedCentralCrossRefGoogle Scholar
  69. Lal A, Edwards GE (1996) Analysis of inhibition of photosynthesis under water stress in the C4 species Amaranthus cruentus and Zea mays: electron transport, CO2 fixation and carboxylation capacity. Aust J Plant Physiol 23:403–412CrossRefGoogle Scholar
  70. Lara MV, Disante KB, Podesta FE, Andreo CS, Drincovich MF (2003) Induction of a Crassulacean acid like metabolism in the C4 succulent plant, Portulaca oleracea L.: physiological and morphological changes are accompanied by specific modifications in phosphoenolpyruvate carboxylase. Photosynth Res 77:241–254PubMedCrossRefGoogle Scholar
  71. Lara MV, Drincovich MF, Andreo CS (2004) Induction of a crassulacean acid-like metabolism in the C4 succulent plant, Portulaca oleracea L.: study of enzymes involved in carbon fixation and carbohydrate metabolism. Plant Cell Physiol 45:618–626PubMedCrossRefGoogle Scholar
  72. Lara MV, Offermann S, Smith M, Okita TW, Andreo CS, Edwards GE (2008) Leaf development in the single-cell C4 system in Bienertia sinuspersici: expression of genes and peptide levels for C4 metabolism in relation to chlorenchyma structure under different light conditions. Plant Physiol 148:593–610PubMedPubMedCentralCrossRefGoogle Scholar
  73. Larkin RM, Stefano G, Ruckle ME, Stavoe AK, Sinkler CA, Brandizzi F et al (2016) REDUCED CHLOROPLAST COVERAGE genes from Arabidopsis thaliana help to establish the size of the chloroplast compartment. Proc Natl Acad Sci U S A 113:E 1116–EE1125CrossRefGoogle Scholar
  74. Lin HC, Karki S, Coe RA, Bagha S, Khoshravesh R, Balahadia CP et al (2016) Targeted knockdown of GDCH in rice leads to a photorespiratory-deficient phenotype useful as a building block for C4 rice. Plant Cell Physiol 57:919–932PubMedCrossRefGoogle Scholar
  75. Longstreth DJ, Hartsock TL, Nobel PS (1980) Mesophyll cell properties for some C3 and C4 species with high photosynthetic rates. Plant Physiol 48:494–498CrossRefGoogle Scholar
  76. Ma JY, Sun W, Koteyeva NK, Voznesenskaya E, Stutz SS, Gandin A et al (2016) Influence of light and nitrogen on the photosynthetic efficiency in the C4 plant Miscanthus x giganteus. Photosynth Res 131:1–13PubMedCrossRefGoogle Scholar
  77. Maai E, Miyake H, Taniguchi M (2011a) Differential positioning of chloroplasts in C4 mesophyll and bundle sheath cells. Plant Signal Behav 6:1111–1113PubMedPubMedCentralCrossRefGoogle Scholar
  78. Maai E, Shimada S, Yamada M, Sugiyama T, Miyake H, Taniguchi M (2011b) The avoidance and aggregative movements of mesophyll chloroplasts in C4 monocots in response to blue light and abscisic acid. J Exp Bot 62:3213–3221PubMedCrossRefGoogle Scholar
  79. McKown AD, Cochard H, Sack L (2010) Decoding leaf hydraulics with a spatially explicit model: principles of venation architecture and implications for its evolution. Am Nat 175:447–460PubMedCrossRefGoogle Scholar
  80. Meinzer FC, Plaut Z, Saliendra NZ (1994) Carbon-isotope discrimination, gas-exchange, and growth of sugarcane cultivars under salinity. Plant Physiol 104:521–526PubMedPubMedCentralCrossRefGoogle Scholar
  81. Mertz RA, Brutnell TP (2014) Bundle sheath suberization in grass leaves: multiple barriers to characterization. J Exp Bot 65:3371–3380PubMedCrossRefGoogle Scholar
  82. Miyake H (2016) Starch accumulation in the bundle sheaths of C3 plants: a possible pre-condition for C4 photosynthesis. Plant Cell Physiol 57:890–896PubMedCrossRefGoogle Scholar
  83. Miyake H, Maeda E (1976) Development of bundle sheath chloroplasts in rice seedlings. Can J Bot 54:556–565CrossRefGoogle Scholar
  84. Miyake H, Maeda E (1978) Starch accumulation in bundle sheath chloroplasts during leaf development of C3 and C4 plants of Gramineae. Can J Bot 56:880–882CrossRefGoogle Scholar
  85. Miyake H, Nakamura M (1993) Some factors concerning the centripetal disposition of bundle sheath chloroplasts during the leaf development of Eleusine coracana. Ann Bot 72:205–211CrossRefGoogle Scholar
  86. Miyake H, Yamamoto Y (1987) Centripetal disposition of bundle sheath chloroplasts during the leaf development of Eleusine coracana. Ann Bot 60:641–647CrossRefGoogle Scholar
  87. Miyake H, Furukawa A, Totsuka T (1985) Structural associations between mitochondria and chloroplasts in the bundle sheath cells of Portulaca Oleracea. Ann Bot 55:815–817CrossRefGoogle Scholar
  88. Muhaidat R, Sage RF, Dengler NG (2007) Diversity of Kranz anatomy and biochemistry in C4 eudicots. Am J Bot 94:362–381CrossRefGoogle Scholar
  89. Muhaidat R, Sage TL, Frohlich M, Dengler NG, Sage RF (2011) Characterization of C3-C4 intermediate species in the genus Heliotropium L. (Boraginaceae): anatomy, ultrastructure and enzyme activity. Plant Cell Environ 34:1723–1736PubMedCrossRefGoogle Scholar
  90. Munekage YN, Taniguchi YY (2016) Promotion of cyclic electron transport around photosystem I with the development of C4 photosynthesis. Plant Cell Physiol 57:897–903PubMedCrossRefGoogle Scholar
  91. Offermann S, Okita TW, Edwards GE (2011) Resolving the compartmentation and function of C4 photosynthesis in the single-cell C4 species Bienertia sinuspersici. Plant Physiol 155:1612–1628PubMedPubMedCentralCrossRefGoogle Scholar
  92. Ohsugi R, Murata T (1980) Leaf anatomy, post-illumination CO2 burst and NAD-malic enzyme activity of Panicum dichotomiflorum. Plant Cell Physiol 21:1329–1333CrossRefGoogle Scholar
  93. Ohsugi R, Samejima M, Chonan N, Murata T (1988) delta13C values and the occurrence of suberized lamellae in some Panicum species. Ann Bot 62:53–59CrossRefGoogle Scholar
  94. Ohsugi R, Ueno O, Komatsu T, Sasaki H, Murata T (1997) Leaf anatomy and carbon discrimination in NAD-malic enzyme Panicum species and their hybrids differing in bundle sheath cell ultrastructure. Ann Bot 79:179–184CrossRefGoogle Scholar
  95. Oikawa K, Matsunaga S, Mano S, Kondo M, Yamada K, Hayashi M et al (2015) Physical interaction between peroxisomes and chloroplasts elucidated by in situ laser analysis. Nat Plants 1:15035PubMedCrossRefGoogle Scholar
  96. Omoto E, Kawasaki M, Taniguchi M, Miyake H (2009) Salinity induces granal development in bundle sheath chloroplasts of NADP-malic enzyme type C4 plants. Plant Prod Sci 12:199–207CrossRefGoogle Scholar
  97. Omoto E, Nagao H, Taniguchi M, Miyake H (2013) Localization of reactive oxygen species and change of antioxidant capacities in mesophyll and bundle sheath chloroplasts of maize under salinity. Physiol Plant 149:1–12PubMedCrossRefGoogle Scholar
  98. Omoto E, Iwasaki Y, Miyake H, Taniguchi M (2016) Salinity induces membrane structure and lipid changes in maize mesophyll and bundle sheath chloroplasts. Physiol Plant 157:13–23PubMedCrossRefGoogle Scholar
  99. Osborn HL, Alonso-Cantabrana H, Sharwood RE, Covshoff S, Evans JR, Furbank RT, von Caemmerer S (2017) Effects of reduced carbonic anhydrase activity on CO2 assimilation rates in Setaria viridis: a transgenic analysis. J Exp Bot 68:299–310PubMedCrossRefGoogle Scholar
  100. Osborne CP, Sack L (2012) Evolution of C4 plants: a new hypothesis for an interaction of CO2 and water relations mediated by plant hydraulics. Philos Trans R Soc Lond Ser B Biol Sci 367:583–600CrossRefGoogle Scholar
  101. Park J, Knoblauch M, Okita T, Edwards G (2009) Structural changes in the vacuole and cytoskeleton are key to development of the two cytoplasmic domains supporting single-cell C4 photosynthesis in Bienertia sinuspersici. Planta 229:369–382PubMedCrossRefGoogle Scholar
  102. Pengelly JJL, Sirault XRR, Tazoe Y, Evans JR, Furbank RT, von Caemmerer S (2010) Growth of the C4 dicot Flaveria bidentis: photosynthetic acclimation to low light through shifts in leaf anatomy and biochemistry. J Exp Bot 61:4109–4122PubMedPubMedCentralCrossRefGoogle Scholar
  103. Perez-Sancho J, Tilsner J, Samuels AL, Botella MA, Bayer EM, Rosado A (2016) Stitching organelles: organization and function of specialized membrane contact sites in plants. Trends Cell Biol 26:705–717PubMedCrossRefGoogle Scholar
  104. Pfeffer M, Peisker M (1998) CO2 gas exchange and phosphenolpyruvate carboxylase activity in leaves of Zea mays L. Photosynth Res 58:281–291CrossRefGoogle Scholar
  105. Prendergast HDV, Hattersley PW, Stone NE (1987) New structural/biochemical associations in leaf blades of C4 grasses (Poaceae). Aust J Plant Physiol 14:403–420CrossRefGoogle Scholar
  106. Rojas-Pierce M, Whippo CW, Davis PA, Hangarter RP, Springer PS (2014) PLASTID MOVEMENT IMPAIRED1 mediates ABA sensitivity during germination and implicates ABA in light-mediated chloroplast movements. Plant Physiol Biochem 83:185–193PubMedCrossRefGoogle Scholar
  107. Sack L, Holbrook NM (2006) Leaf hydraulics. Annu Rev Plant Biol 57:361–381PubMedCrossRefGoogle Scholar
  108. Sack L, Scoffoni C (2013) Leaf venation: structure, function, development, evolution, ecology and applications in the past, present and future. New Phytol 198:983–1000PubMedCrossRefGoogle Scholar
  109. Sage RF (2001) Environmental and evolutionary preconditions for the origin and diversification of the C4 photosynthetic syndrome. Plant Biol 3:202–213CrossRefGoogle Scholar
  110. Sage R (2002) C4 photosynthesis in terrestrial plants does not require Kranz anatomy. Trends Plant Sci 7:283–285PubMedCrossRefGoogle Scholar
  111. Sage TL, Sage RF (2009) The functional anatomy of rice leaves: implications for refixation of photorespiratory CO2 and efforts to engineer C4 photosynthesis into rice. Plant Cell Physiol 50:756–772PubMedCrossRefGoogle Scholar
  112. Sage RF, Christin PA, Edwards EJ (2011a) The C4 plant lineages of planet Earth. J Exp Bot 62:3155–3169CrossRefGoogle Scholar
  113. Sage TL, Sage RF, Vogan PJ, Rahman B, Johnson DC, Oakley JC, Heckel MA (2011b) The occurrence of C2 photosynthesis in Euphorbia subgenus Chamaesyce (Euphorbiaceae). J Exp Bot 62:3183–3195PubMedCrossRefGoogle Scholar
  114. Sage RF, Sage TL, Kocacinar F (2012) Photorespiration and the evolution of C4 photosynthesis. Annu Rev Plant Biol 63:19–47PubMedCrossRefGoogle Scholar
  115. Sage TL, Busch FA, Johnson DC, Friesen PC, Stinson CR, Stata M et al (2013) Initial events during the evolution of C4 photosynthesis in C3 species of Flaveria. Plant Physiol 163:1266–1276PubMedPubMedCentralCrossRefGoogle Scholar
  116. Sage RF, Khoshravesh R, Sage TL (2014) From proto-Kranz to C4 Kranz: building the bridge to C4 photosynthesis. J Exp Bot 65:3341–3356PubMedCrossRefGoogle Scholar
  117. Sakai Y, Takagi S (2005) Reorganized actin filaments anchor chloroplasts along the anticlinal walls of Vallisneria epidermal cells under high-intensity blue light. Planta 221:823–830PubMedCrossRefGoogle Scholar
  118. Slewinski TL (2013) Using evolution as a guide to engineer Kranz-type C4 photosynthesis. Front Plant Sci 4:212PubMedPubMedCentralGoogle Scholar
  119. Stata M, Sage TL, Rennie TD, Khoshravesh R, Sultmanis S, Khaikin Y et al (2014) Mesophyll cells of C4 plants have fewer chloroplasts than those of closely related C3 plants. Plant Cell Environ 37:2587–2600PubMedCrossRefGoogle Scholar
  120. Stata M, Sage TL, Hoffmann N, Covshoff S, Ka-Shu Wong G, Sage RF (2016) Mesophyll chloroplast investment in C3, C4 and C2 species of the genus Flaveria. Plant Cell Physiol 57:904–918PubMedCrossRefGoogle Scholar
  121. Stutz SS, Edwards GE, Cousins AB (2014) Single-cell C4 photosynthesis: efficiency and acclimation of Bienertia sinuspersici to growth under low light. New Phytol 202:220–232PubMedCrossRefGoogle Scholar
  122. Takagi S (2003) Actin-based photo-orientation movement of chloroplasts in plant cells. J Exp Biol 206:1963–1969PubMedCrossRefGoogle Scholar
  123. Takagi S, Takamatsu H, Sakurai-Ozato N (2009) Chloroplast anchoring: its implications for the regulation of intracellular chloroplast distribution. J Exp Bot 60:3301–3310PubMedCrossRefGoogle Scholar
  124. Taniguchi M, Sugiyama T (1997) The expression of 2-oxoglutarate/malate translocator in the bundle-sheath mitochondria of Panicum miliaceum, a NAD-malic enzyme-type C4 plant, is regulated by light and development. Plant Physiol 114:285–293PubMedPubMedCentralCrossRefGoogle Scholar
  125. Taniguchi Y, Taniguchi M, Kawasaki M, Miyake H (2003) Strictness of the centrifugal location of bundle sheath chloroplasts in different NADP-ME type C4 grasses. Plant Prod Sci 6:274–280CrossRefGoogle Scholar
  126. Tazoe Y, von Caemmerer S, Estavillo GM, Evans JR (2011) Using tunable diode laser spectroscopy to measure carbon isotope discrimination and mesophyll conductance to CO2 diffusion dynamically at different CO2 concentrations. Plant Cell Environ 34:580–591PubMedCrossRefGoogle Scholar
  127. Tolley BJ, Sage TL, Langdale JA, Hibberd JM (2012) Individual maize chromosomes in the C3 plant oat can increase bundle sheath cell size and vein density. Plant Physiol 159:1418–1427PubMedPubMedCentralCrossRefGoogle Scholar
  128. Ubierna N, Gandin A, Boyd RA, Cousins AB (2017) Temperature response of mesophyll conductance in three C4 species calculated with two. Methods: 18O discrimination and in vitro V pmax. New Phytol 214:66–80PubMedCrossRefGoogle Scholar
  129. Ueno O (1998) Induction of Kranz anatomy and C4-like biochemical characteristics in a submerged amphibious plant by abscisic acid. Plant Cell 10:571–583PubMedPubMedCentralGoogle Scholar
  130. von Caemmerer S (2000) Biochemical models of leaf photosynthesis. CSIRO publishing, CollingwoodGoogle Scholar
  131. von Caemmerer S, Furbank RT (2003) The C4 pathway: an efficient CO2 pump. Photosynth Res 77:191–207CrossRefGoogle Scholar
  132. von Caemmerer S, Ludwig M, Millgate A, Farquhar GD, Price D, Badger M, Furbank RT (1997) Carbon isotope discrimination during C4 photosynthesis: insights from transgenic plants. Aust J Plant Physiol 24:487–494CrossRefGoogle Scholar
  133. von Caemmerer S, Hendrickson L, Quinn V, Vella N, Millgate AG, Furbank RT (2005) Reductions of Rubisco activase by antisense RNA in the C4 plant Flaveria bidentis reduces Rubisco carbamylation and leaf photosynthesis. Plant Physiol 137:747–755CrossRefGoogle Scholar
  134. von Caemmerer S, Edwards GE, Koteyeva NK, Cousins AB (2014a) Single cell C4 photosynthesis in aquatic and terrestrial plants: a gas exchange perspective. Aquat Bot 118:71–80CrossRefGoogle Scholar
  135. von Caemmerer S, Ghannoum O, Pengelly JJ, Cousins AB (2014b) Carbon isotope discrimination as a tool to explore C4 photosynthesis. J Exp Bot 65:3459–3470CrossRefGoogle Scholar
  136. Voznesenskaya EV, Franceschi VR, Kiirats O, Freitag H, Edwards GE (2001) Kranz anatomy is not essential for terrestrial C4 plant photosynthesis. Nature 414:543–546PubMedCrossRefGoogle Scholar
  137. Voznesenskaya EV, Franceschi VR, Kiirats O, Artyusheva EG, Freitag H, Edwards GE (2002) Proof of C4 photosynthesis without Kranz anatomy in Bienertia cycloptera (Chenopodiaceae). Plant J 31:649–662PubMedCrossRefGoogle Scholar
  138. Voznesenskaya EV, Koteyeva NK, Chuong SD, Akhani H, Edwards GE, Franceschi VR (2005) Differentiation of cellular and biochemical features of the single-cell C4 syndrome during leaf development in Bienertia cycloptera (Chenopodiaceae). Am J Bot 92:1784–1795PubMedCrossRefGoogle Scholar
  139. Voznesenskaya EV, Franceschi VR, Chuong SD, Edwards GE (2006) Functional characterization of phosphoenolpyruvate carboxykinase-type C4 leaf anatomy: immuno-, cytochemical and ultrastructural analyses. Ann Bot 98:77–91PubMedPubMedCentralCrossRefGoogle Scholar
  140. Wada M, Kagawa T, Sato Y (2003) Chloroplast movement. Annu Rev Plant Biol 24:455–468CrossRefGoogle Scholar
  141. Wang Y, Brautigam A, Weber AP, Zhu XG (2014a) Three distinct biochemical subtypes of C4 photosynthesis? A modelling analysis. J Exp Bot 65:3567–3578PubMedPubMedCentralCrossRefGoogle Scholar
  142. Wang Y, Long SP, Zhu XG (2014b) Elements required for an efficient NADP-malic enzyme type C4 photosynthesis. Plant Physiol 164:2231–2246PubMedPubMedCentralCrossRefGoogle Scholar
  143. Weiner H, Burnell JN, Woodrow IE, Heldt HW, Hatch MD (1988) Metabolite diffusion into bundle sheath cells from C4 plants: relation to C4 photosynthesis and plasmodesmatal function. Plant Physiol 88:815–822PubMedPubMedCentralCrossRefGoogle Scholar
  144. Williams DG, Gempko V, Fravolini A, Leavitt SW, Wall GW, Kimball PA, Pinter PJ, LaMorte R (2001) Carbon isotope discrimination by Sorghum bicolor under CO2 enrichment and drought. New Phytol 150:285–293CrossRefGoogle Scholar
  145. Yamada M, Kawasaki M, Sugiyama T, Miyake H, Taniguchi M (2009) Differential positioning of C4 mesophyll and bundle sheath chloroplasts: aggregative movement of C4 mesophyll chloroplasts in response to environmental stresses. Plant Cell Physiol 50:1736–1749PubMedCrossRefGoogle Scholar
  146. Yamane K, Hayakawa K, Kawasaki M, Taniguchi M, Miyake H (2003) Bundle sheath chloroplasts of rice are more sensitive to drought stress than mesophyll chloroplasts. J Plant Physiol 160:1319–1327PubMedCrossRefGoogle Scholar
  147. Yoshimura Y, Kubota F, Ueno O (2004) Structural and biochemical bases of photorespiration in C4 plants: quantification of organelles and glycine decarboxylase. Planta 220:307–317PubMedCrossRefGoogle Scholar
  148. Zhang JH, Jia WS, Yang JC, Ismail AM (2006) Role of ABA in integrating plant responses to drought and salt stresses. Field Crop Res 97:111–119CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Graduate School of Bioagricultural SciencesNagoya UniversityNagoyaJapan
  2. 2.School of Biological SciencesWashington State University PullmanPullmanUSA

Personalised recommendations