Photosynthesis Research

, Volume 119, Issue 1–2, pp 157–167 | Cite as

Getting the most out of natural variation in C4 photosynthesis

  • Sarah Covshoff
  • Steven J. Burgess
  • Jana Kneřová
  • Britta M. C. Kümpers
Review

Abstract

C4 photosynthesis is a complex trait that has a high degree of natural variation, involving anatomical and biochemical changes relative to the ancestral C3 state. It has evolved at least 66 times across a variety of lineages and the evolutionary route from C3 to C4 is likely conserved but not necessarily genetically identical. As such, a variety of C4 species are needed to identify what is fundamental to the C4 evolutionary process in a global context. In order to identify the genetic components of C4 form and function, a number of species are used as genetic models. These include Zea mays (maize), Sorghumbicolor (sorghum), Setaria viridis (Setaria), Flaveria bidentis, and Cleome gynandra. Each of these species has different benefits and challenges associated with its use as a model organism. Here, we propose that RNA profiling of a large sampling of C4, C3–C4, and C3 species, from as many lineages as possible, will allow identification of candidate genes necessary and sufficient to confer C4 anatomy and/or biochemistry. Furthermore, C4 model species will play a critical role in the functional characterization of these candidate genes and identification of their regulatory elements, by providing a platform for transformation and through the use of gene expression profiles in mesophyll and bundle sheath cells and along the leaf developmental gradient. Efforts should be made to sequence the genomes of F. bidentis and C. gynandra and to develop congeneric C3 species as genetic models for comparative studies. In combination, such resources would facilitate discovery of common and unique C4 regulatory mechanisms across genera.

Keywords

C4 photosynthesis Maize Sorghum Flaveria Setaria viridis Cleome gynandra 

References

  1. Akyildiz M, Gowik U, Engelmann S, Koczor M, Streubel M, Westhoff P (2007) Evolution and function of a cis-regulatory module for mesophyll-specific gene expression in the C4 dicot Flaveria trinervia. Plant Cell 19(11):3391–3402PubMedCentralPubMedGoogle Scholar
  2. Bennetzen JL, Schmutz J, Wang H, Percifield R, Hawkins J, Pontaroli AC, Estep M, Feng L, Vaughn JN, Grimwood J, Jenkins J, Barry K, Lindquist E, Hellsten U, Deshpande S, Wang X, Wu X, Mitros T, Triplett J, Yang X, Ye CY, Mauro-Herrera M, Wang L, Li P, Sharma M, Sharma R, Ronald PC, Panaud O, Kellogg EA, Brutnell TP, Doust AN, Tuskan GA, Rokhsar D, Devos KM (2012) Reference genome sequence of the model plant Setaria. Nat Biotechnol 30(6):555–561PubMedGoogle Scholar
  3. Bevan M, Walsh S (2005) The Arabidopsis genome: a foundation for plant research. Genome Res 15(12):1632–1642PubMedGoogle Scholar
  4. Bouton JH, Brown RH, Byrd GT, Sharkey TD (1990) Inheritance of the reversal of O2 response of photosynthesis in a Flaveria linearis mutant. Plant Physiol 92(1):186–190PubMedCentralPubMedGoogle Scholar
  5. Bräutigam A, Kajala K, Wullenweber J, Sommer M, Gagneul D, Weber KL, Carr KM, Gowik U, Mass J, Lercher MJ, Westhoff P, Hibberd JM, Weber AP (2011) An mRNA blueprint for C4 photosynthesis derived from comparative transcriptomics of closely related C3 and C4 species. Plant Physiol 155(1):142–156PubMedCentralPubMedGoogle Scholar
  6. Brown HR, Bouton JH (1993) Physiology and genetics of interspecific hybrids between photosynthetic types. Annu Rev Plant Physiol Plant Mol Biol 44:435–456Google Scholar
  7. Brown RH, Byrd GT (1993) Estimation of bundle sheath cell conductance in C4 species and O2 insensitivity of photosynthesis. Plant Physiol 103(4):1183–1188PubMedCentralPubMedGoogle Scholar
  8. Brown NJ, Parsley K, Hibberd JM (2005) The future of C4 research–maize, Flaveria or Cleome? Trends Plant Sci 10(5):215–221PubMedGoogle Scholar
  9. Brown NJ, Newell CA, Stanley S, Chen JE, Perrin AJ, Kajala K, Hibberd JM (2011) Independent and parallel recruitment of preexisting mechanisms underlying C4 photosynthesis. Science 331(6023):1436–1439PubMedGoogle Scholar
  10. Brutnell TP, Wang L, Swartwood K, Goldschmidt A, Jackson D, Zhu XG, Kellogg E, Van Eck J (2010) Setaria viridis: a model for C4 photosynthesis. Plant Cell 22(8):2537–2544PubMedCentralPubMedGoogle Scholar
  11. Byrt CS, Grof CP, Furbank RT (2011) C4 plants as biofuel feedstocks: optimising biomass production and feedstock quality from a lignocellulosic perspective. J Integr Plant Biol 53(2):120–135PubMedGoogle Scholar
  12. Cameron RG, Bassett CL, Bouton JH, Brown RH (1989) Transfer of C4 photosynthetic characters through hybridization of Flaveria species. Plant Physiol 90(4):1538–1545PubMedCentralPubMedGoogle Scholar
  13. Carpita NC, McCann MC (2008) Maize and sorghum: genetic resources for bioenergy grasses. Trends Plant Sci 13(8):415–420PubMedGoogle Scholar
  14. Chang YM, Liu WY, Shih AC, Shen MN, Lu CH, Lu MY, Yang HW, Wang TY, Chen SC, Chen SM, Li WH, Ku MS (2012) Characterizing regulatory and functional differentiation between maize mesophyll and bundle sheath cells by transcriptomic analysis. Plant Physiol 160(1):165–177PubMedCentralPubMedGoogle Scholar
  15. Chitty JA, Furbank RT, Marshall JS, Chen Z, Taylor WC (1994) Genetic transformation of the C4 plant Flaveria bidentis. Plant J 6(6):949–956Google Scholar
  16. Covshoff S, Hibberd JM (2012) Integrating C4 photosynthesis into C3 crops to increase yield potential. Curr Opin Biotechnol 23(2):209–214PubMedGoogle Scholar
  17. Covshoff S, Majeran W, Liu P, Kolkman JM, van Wijk KJ, Brutnell TP (2008) Deregulation of maize C4 photosynthetic development in a mesophyll cell-defective mutant. Plant Physiol 146(4):1469–1481PubMedCentralPubMedGoogle Scholar
  18. Covshoff S, Furbank RT, Leegood RC, Hibberd JM (2013) Leaf rolling allows quantification of mRNA abundance in mesophyll cells of sorghum. J Exp Bot 64(3):807–813PubMedGoogle Scholar
  19. Doust AN, Kellogg EA, Devos KM, Bennetzen JL (2009) Foxtail millet: a sequence-driven grass model system. Plant Physiol 149(1):137–141PubMedCentralPubMedGoogle Scholar
  20. Edwards GE, Voznesenskaya EV (2011) C4 photosynthesis: Kranz forms and single-cell C4 in terrestrial plants. In: Raghavendra AS, Sage RF (eds) Photosynthesis and related CO2 concentrating mechanisms. Advances in Photosynthesis Research. Kluwer Academic Publishers, Dordrecht, pp 29–60Google Scholar
  21. Engelmann S, Zogel C, Koczor M, Schlue U, Streubel M, Westhoff P (2008) Evolution of the C4 phosphoenolpyruvate carboxylase promoter of the C4 species Flaveria trinervia: the role of the proximal promoter region. BMC Plant Biol 8:4Google Scholar
  22. Friso G, Majeran W, Huang M, Sun Q, van Wijk KJ (2010) Reconstruction of metabolic pathways, protein expression, and homeostasis machineries across maize bundle sheath and mesophyll chloroplasts: large-scale quantitative proteomics using the first maize genome assembly. Plant Physiol 152(3):1219–1250PubMedCentralPubMedGoogle Scholar
  23. Furbank RT (2011) Evolution of the C4 photosynthetic mechanism: are there really three C4 acid decarboxylation types? J Exp Bot 62(9):3103–3108PubMedGoogle Scholar
  24. Furbank RT, Chitty JA, von Caemmerer S, Jenkins C (1996) Antisense RNA inhibition of RbcS gene expression reduces Rubisco level and photosynthesis in the C4 plant Flaveria bidentis. Plant Physiol 111(3):725–734PubMedCentralPubMedGoogle Scholar
  25. Furumoto T, Hata S, Izui K (2000) Isolation and characterization of cDNAs for differentially accumulated transcripts between mesophyll cells and bundle sheath strands of maize leaves. Plant Cell Physiol 41(11):1200–1209PubMedGoogle Scholar
  26. Furumoto T, Izui K, Quinn V, Furbank RT, von Caemmerer S (2007) Phosphorylation of phosphoenolpyruvate carboxylase is not essential for high photosynthetic rates in the C4 species Flaveria bidentis. Plant Physiol 144(4):1936–1945PubMedCentralPubMedGoogle Scholar
  27. Furumoto T, Yamaguchi T, Ohshima-Ichie Y, Nakamura M, Tsuchida-Iwata Y, Shimamura M, Ohnishi J, Hata S, Gowik U, Westhoff P, Bräutigam A, Weber AP, Izui K (2011) A plastidial sodium-dependent pyruvate transporter. Nature 476(7361):472–475PubMedGoogle Scholar
  28. Gowik U, Westhoff P (2011) The path from C3 to C4 photosynthesis. Plant Physiol 155(1):56–63PubMedCentralPubMedGoogle Scholar
  29. Gowik U, Bräutigam A, Weber KL, Weber AP, Westhoff P (2011) Evolution of C4 photosynthesis in the genus Flaveria: how many and which genes does it take to make C4? Plant Cell 23(6):2087–2105PubMedCentralPubMedGoogle Scholar
  30. Hatch MD (1987) C4 photosynthesis: a unique blend of modified biochemistry, anatomy and ultrastructure. Biochim Biophys Acta 895:81–106Google Scholar
  31. Heaton E, Voigt T, Long SP (2004) A quantitative review comparing the yields of two candidate C4 perennial biomass crops in relation to nitrogen, temperature and water. Biomass Bioenerg 27(1):21–30Google Scholar
  32. Hibberd JM, Covshoff S (2010) The regulation of gene expression required for C4 photosynthesis. Annu Rev Plant Biol 61:181–207PubMedGoogle Scholar
  33. Hibberd JM, Sheehy JE, Langdale JA (2008) Using C4 photosynthesis to increase the yield of rice-rationale and feasibility. Curr Opin Plant Biol 11(2):228–231PubMedGoogle Scholar
  34. Holaday AS, Brown RH, Bartlett JM, Sandlin EA, Jackson RC (1988) Enzymic and photosynthetic characteristics of reciprocal F1 hybrids of Flaveria pringlei (C3) and Flaveria brownii (C4-like species). Plant Physiol 87(2):484–490PubMedCentralPubMedGoogle Scholar
  35. Huber WE, Brown RH, Bouton JH, Sternberg LO (1989) CO2 exchange, cytogenetics, and leaf anatomy of hybrids between photosynthetically distinct Flaveria species. Plant Physiol 89(3):839–844PubMedCentralPubMedGoogle Scholar
  36. Iltis HH, Cochrane TS (2007) Studies in the Cleomaceae V: a new genus and ten new combinations for the flora of North America. Novon 17(4):447–451Google Scholar
  37. Jacobs B, Engelmann S, Westhoff P, Gowik U (2008) Evolution of C4 phosphoenolpyruvate carboxylase in Flaveria: determinants for high tolerance towards the inhibitor l-malate. Plant Cell Environ 31(6):793–803PubMedGoogle Scholar
  38. Jiao Y, Tausta SL, Gandotra N, Sun N, Liu T, Clay NK, Ceserani T, Chen M, Ma L, Holford M, Zhang HY, Zhao H, Deng XW, Nelson T (2009) A transcriptome atlas of rice cell types uncovers cellular, functional and developmental hierarchies. Nat Genet 41(2):258–263PubMedGoogle Scholar
  39. Johnson MT, Carpenter EJ, Tian Z, Bruskiewich R, Burris JN, Carrigan CT, Chase MW, Clarke ND, Covshoff S, Depamphilis CW, Edger PP, Goh F, Graham S, Greiner S, Hibberd JM, Jordon-Thaden I, Kutchan TM, Leebens-Mack J, Melkonian M, Miles N, Myburg H, Patterson J, Pires JC, Ralph P, Rolf M, Sage RF, Soltis D, Soltis P, Stevenson D, Stewart CN Jr, Surek B, Thomsen CJ, Villarreal JC, Wu X, Zhang Y, Deyholos MK, Wong GK (2012) Evaluating methods for isolating total RNA and predicting the success of sequencing phylogenetically diverse plant transcriptomes. PLoS One 7(11):e50226PubMedCentralPubMedGoogle Scholar
  40. Kajala K, Covshoff S, Karki S, Woodfield H, Tolley BJ, Dionora MJ, Mogul RT, Mabilangan AE, Danila FR, Hibberd JM, Quick WP (2011) Strategies for engineering a two-celled C4 photosynthetic pathway into rice. J Exp Bot 62(9):3001–3010PubMedGoogle Scholar
  41. Kajala K, Brown NJ, Williams BP, Borrill P, Taylor LE, Hibberd JM (2012) Multiple Arabidopsis genes primed for recruitment into C4 photosynthesis. Plant J 69(1):47–56PubMedGoogle Scholar
  42. Kolkman JM, Conrad LJ, Farmer PR, Hardeman K, Ahern KR, Lewis PE, Sawers RJ, Lebejko S, Chomet P, Brutnell TP (2005) Distribution of Activator (Ac) throughout the maize genome for use in regional mutagenesis. Genetics 169(2):981–995PubMedGoogle Scholar
  43. Koornneef M, Meinke D (2010) The development of Arabidopsis as a model plant. Plant J 61(6):909–921PubMedGoogle Scholar
  44. Koteyeva NK, Voznesenskaya EV, Roalson EH, Edwards GE (2011) Diversity in forms of C4 in the genus Cleome (Cleomaceae). Ann Bot 107(2):269–283PubMedGoogle Scholar
  45. Lai LB, Wang L, Nelson TM (2002) Distinct but conserved functions for two chloroplastic NADP-malic enzyme isoforms in C3 and C4 Flaveria species. Plant Physiol 128(1):125–139PubMedCentralPubMedGoogle Scholar
  46. Langdale JA (2011) C4 cycles: past, present, and future research on C4 photosynthesis. Plant Cell 23(11):3879–3892PubMedCentralPubMedGoogle Scholar
  47. Lara MV, Casati P, Andreo CS (2002) CO2-concentrating mechanisms in Egeria densa, a submersed aquatic plant. Physiol Plant 115(4):487–495PubMedGoogle Scholar
  48. Li P, Brutnell TP (2011) Setaria viridis and Setaria italica, model genetic systems for the Panicoid grasses. J Exp Bot 62(9):3031–3037PubMedGoogle Scholar
  49. Li P, Ponnala L, Gandotra N, Wang L, Si Y, Tausta SL, Kebrom TH, Provart N, Patel R, Myers CR, Reidel EJ, Turgeon R, Liu P, Sun Q, Nelson T, Brutnell TP (2010) The developmental dynamics of the maize leaf transcriptome. Nat Genet 42(12):1060–1067PubMedGoogle Scholar
  50. Liu WY, Chang YM, Chen SC, Lu CH, Wu YH, Lu MY, Chen DR, Shih AC, Sheue CR, Huang HC, Yu CP, Lin HH, Shiu SH, Ku MS, Li WH (2013) Anatomical and transcriptional dynamics of maize embryonic leaves during seed germination. PNAS 110(10):3979–3984PubMedGoogle Scholar
  51. Long SP, Zhu XG, Naidu SL, Ort DR (2006) Can improvement in photosynthesis increase crop yields? Plant Cell Environ 29(3):315–330PubMedGoogle Scholar
  52. Ludwig M (2011) The molecular evolution of β-carbonic anhydrase in Flaveria. J Exp Bot 62(9):3071–3081PubMedGoogle Scholar
  53. Ludwig M, von Caemmerer S, Dean Price G, Badger MR, Furbank RT (1998) Expression of tobacco carbonic anhydrase in the C4 dicot Flaveria bidentis leads to increased leakiness of the bundle sheath and a defective CO2-concentrating mechanism. Plant Physiol 117(3):1071–1081PubMedCentralPubMedGoogle Scholar
  54. Magnin NC, Cooley BA, Reiskind JB, Bowes G (1997) Regulation and localization of key enzymes during the induction of Kranz-less, C4-type photosynthesis in Hydrilla verticillata. Plant Physiol 115(4):1681–1689PubMedCentralPubMedGoogle Scholar
  55. Majeran W, Cai Y, Sun Q, van Wijk KJ (2005) Functional differentiation of bundle sheath and mesophyll maize chloroplasts determined by comparative proteomics. Plant Cell 17(11):3111–3140PubMedCentralPubMedGoogle Scholar
  56. Majeran W, Friso G, Ponnala L, Connolly B, Huang M, Reidel E, Zhang C, Asakura Y, Bhuiyan NH, Sun Q, Turgeon R, van Wijk KJ (2010) Structural and metabolic transitions of C4 leaf development and differentiation defined by microscopy and quantitative proteomics in maize. Plant Cell 22(11):3509–3542PubMedCentralPubMedGoogle Scholar
  57. Marshall JS, Stubbs JD, Chitty JA, Surin B, Taylor WC (1997) Expression of the C4 Me1 gene from Flaveria bidentis requires an interaction between 5′ and 3′ sequences. Plant Cell 9(9):1515–1525PubMedCentralPubMedGoogle Scholar
  58. 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(5):886–896PubMedGoogle Scholar
  59. McKown AD, Dengler NG (2007) Key innovations in the evolution of Kranz anatomy and C4 vein pattern in Flaveria (Asteraceae). Am J Bot 94(3):382–399PubMedGoogle Scholar
  60. McKown AD, Moncalvo JM, Dengler NG (2005) Phylogeny of Flaveria (Asteraceae) and inference of C4 photosynthesis evolution. Am J Bot 92(11):1911–1928PubMedGoogle Scholar
  61. Meinke DW, Cherry JM, Dean C, Rounsley SD, Koornneef M (1998) Arabidopsis thaliana: a model plant for genome analysis. Science 282(5389):662–682PubMedGoogle Scholar
  62. Meister M, Agostino A, Hatch MD (1996) The roles of malate and aspartate in C4 photosynthetic metabolism of Flaveria bidentis (L.). Planta 199:262–269Google Scholar
  63. Mitchell PL, Sheehy JE (2006) Supercharging rice photosynthesis to increase yield. New Phytol 171(4):688–693PubMedGoogle Scholar
  64. Muhaidat R, Sage RF, Dengler NG (2007) Diversity of Kranz anatomy and biochemistry in C4 eudicots. Am J Bot 94(3):362–381PubMedGoogle Scholar
  65. Nakano Y, Edwards GE (1987) Hill reaction, hydrogen peroxide scavenging, and ascorbate peroxidase activity of mesophyll and bundle sheath chloroplasts of NADP-malic enzyme type C4 species. Plant Physiol 85(1):294–298PubMedCentralPubMedGoogle Scholar
  66. Nelson T, Langdale JA (1992) Developmental genetics of C4 photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 43:25–47Google Scholar
  67. Newell CA, Brown NJ, Liu Z, Pflug A, Gowik U, Westhoff P, Hibberd JM (2010) Agrobacterium tumefaciens-mediated transformation of Cleome gynandra L., a C4 dicotyledon that is closely related to Arabidopsis thaliana. J Exp Bot 61(5):1311–1319PubMedGoogle Scholar
  68. Osmond CB, Björkman O, Anderson DJ (1980) Physiological processes in plant ecology: toward a synthesis with Atriplex. Springer, BerlinGoogle Scholar
  69. Patel M, Siegel AJ, Berry JO (2006) Untranslated regions of FbRbcS1 mRNA mediate bundle sheath cell-specific gene expression in leaves of a C4 plant. J Biol Chem 281(35):25485–25491PubMedGoogle Scholar
  70. Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A, Schmutz J, Spannagl M, Tang H, Wang X, Wicker T, Bharti AK, Chapman J, Feltus FA, Gowik U, Grigoriev IV, Lyons E, Maher CA, Martis M, Narechania A, Otillar RP, Penning BW, Salamov AA, Wang Y, Zhang L, Carpita NC, Freeling M, Gingle AR, Hash CT, Keller B, Klein P, Kresovich S, McCann MC, Ming R, Peterson DG, Mehboob-ur-Rahman, Ware D, Westhoff P, Mayer KF, Messing J, Rokhsar DS (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457(7229):551–556Google Scholar
  71. Pengelly JJ, Kwasny S, Bala S, Evans JR, Voznesenskaya EV, Koteyeva NK, Edwards GE, Furbank RT, von Caemmerer S (2011) Functional analysis of corn husk photosynthesis. Plant Physiol 156(2):503–513PubMedCentralPubMedGoogle Scholar
  72. Pengelly JJ, Tan J, Furbank RT, von Caemmerer S (2012) Antisense reduction of NADP-malic enzyme in Flaveria bidentis reduces flow of CO2 through the C4 cycle. Plant Physiol 160(2):1070–1080PubMedCentralPubMedGoogle Scholar
  73. Pick TR, Bräutigam A, Schlüter U, Denton AK, Colmsee C, Scholz U, Fahnenstich H, Pieruschka R, Rascher U, Sonnewald U, Weber AP (2011) Systems analysis of a maize leaf developmental gradient redefines the current C4 model and provides candidates for regulation. Plant Cell 23(12):4208–4220PubMedCentralPubMedGoogle Scholar
  74. Powell AM (1978) Systematics of Flaveria (Flaveriinae–Asteraceae). Ann Missouri Bot Gard 65(2):590–636Google Scholar
  75. Sage RF (2004) The evolution of C4 photosynthesis. New Phytol 161(2):341–370Google Scholar
  76. Sage RF, Zhu XG (2011) Exploiting the engine of C4 photosynthesis. J Exp Bot 62(9):2989–3000PubMedGoogle Scholar
  77. Sage RF, Sage TL, Pearcy RW, Borsch T (2007) The taxonomic distribution of C4 photosynthesis in Amaranthaceae sensu stricto. Am J Bot 94(12):1992–2003PubMedGoogle Scholar
  78. Sage RF, Christin PA, Edwards EJ (2011) The C4 plant lineages of planet Earth. J Exp Bot 62(9):3155–3169PubMedGoogle Scholar
  79. Sage RF, Sage TL, Kocacinar F (2012) Photorespiration and the evolution of C4 photosynthesis. Annu Rev Plant Biol 63:19–47PubMedGoogle Scholar
  80. Sawers RJ, Liu P, Anufrikova K, Hwang JT, Brutnell TP (2007) A multi-treatment experimental system to examine photosynthetic differentiation in the maize leaf. BMC Genomics 8:12PubMedCentralPubMedGoogle Scholar
  81. Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, Liang C, Zhang J, Fulton L, Graves TA, Minx P, Reily AD, Courtney L, Kruchowski SS, Tomlinson C, Strong C, Delehaunty K, Fronick C, Courtney B, Rock SM, Belter E, Du F, Kim K, Abbott RM, Cotton M, Levy A, Marchetto P, Ochoa K, Jackson SM, Gillam B, Chen W, Yan L, Higginbotham J, Cardenas M, Waligorski J, Applebaum E, Phelps L, Falcone J, Kanchi K, Thane T, Scimone A, Thane N, Henke J, Wang T, Ruppert J, Shah N, Rotter K, Hodges J, Ingenthron E, Cordes M, Kohlberg S, Sgro J, Delgado B, Mead K, Chinwalla A, Leonard S, Crouse K, Collura K, Kudrna D, Currie J, He R, Angelova A, Rajasekar S, Mueller T, Lomeli R, Scara G, Ko A, Delaney K, Wissotski M, Lopez G, Campos D, Braidotti M, Ashley E, Golser W, Kim H, Lee S, Lin J, Dujmic Z, Kim W, Talag J, Zuccolo A, Fan C, Sebastian A, Kramer M, Spiegel L, Nascimento L, Zutavern T, Miller B, Ambroise C, Muller S, Spooner W, Narechania A, Ren L, Wei S, Kumari S, Faga B, Levy MJ, McMahan L, Van Buren P, Vaughn MW, Ying K, Yeh CT, Emrich SJ, Jia Y, Kalyanaraman A, Hsia AP, Barbazuk WB, Baucom RS, Brutnell TP, Carpita NC, Chaparro C, Chia JM, Deragon JM, Estill JC, Fu Y, Jeddeloh JA, Han Y, Lee H, Li P, Lisch DR, Liu S, Liu Z, Nagel DH, McCann MC, SanMiguel P, Myers AM, Nettleton D, Nguyen J, Penning BW, Ponnala L, Schneider KL, Schwartz DC, Sharma A, Soderlund C, Springer NM, Sun Q, Wang H, Waterman M, Westerman R, Wolfgruber TK, Yang L, Yu Y, Zhang L, Zhou S, Zhu Q, Bennetzen JL, Dawe RK, Jiang J, Jiang N, Presting GG, Wessler SR, Aluru S, Martienssen RA, Clifton SW, McCombie WR, Wing RA, Wilson RK (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326(5956):1112–1115PubMedGoogle Scholar
  82. Sharpe RM, Offermann S (2013) One decade after the discovery of single-cell C4 species in terrestrial plants: what did we learn about the minimal requirements of C4 photosynthesis? Photosynth Res. doi:10.1007/s11120-013-9810-9 PubMedGoogle Scholar
  83. Sharpe RM, Mahajan A, Takacs EM, Stern DB, Cahoon AB (2011) Developmental and cell type characterization of bundle sheath and mesophyll chloroplast transcript abundance in maize. Curr Genet 57(2):89–102PubMedGoogle Scholar
  84. Sheen J (1999) C4 gene expression. Annu Rev Plant Physiol Plant Mol Biol 50:187–217PubMedGoogle Scholar
  85. Slack CR, Hatch MD (1967) Comparative studies on the activity of carboxylases and other enzymes in relation to the new pathway of photosynthetic carbon dioxide fixation in tropical grasses. Biochem J 103(3):660–665PubMedGoogle Scholar
  86. Stockhaus J, Poetsch W, Steinmüller K, Westhoff P (1994) Evolution of the C4 phosphoenolpyruvate carboxylase promoter of the C4 dicot Flaveria trinervia: an expression analysis in the C3 plant tobacco. Mol Gen Genet 245(3):286–293PubMedGoogle Scholar
  87. Tanz SK, Tetu SG, Vella NG, Ludwig M (2009) Loss of the transit peptide and an increase in gene expression of an ancestral chloroplastic carbonic anhydrase were instrumental in the evolution of the cytosolic C4 carbonic anhydrase in Flaveria. Plant Physiol 150(3):1515–1529PubMedCentralPubMedGoogle Scholar
  88. The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815Google Scholar
  89. Tsai YT, Chen PY, To KY (2012) Plant regeneration and stable transformation in the floricultural plant Cleome spinosa, a C3 plant closely related to the C4 plant C. gynandra. Plant Cell Rep 31(7):1189–1198PubMedGoogle Scholar
  90. Ueno O, Samejima M, Muto S, Miyachi S (1988) Photosynthetic characteristics of an amphibious plant, Eleocharis vivipara: expression of C4 and C3 modes in contrasting environments. Proc Natl Acad Sci USA 85(18):6733–6737PubMedGoogle Scholar
  91. van der Weijde T, Alvim Kamei CL, Torres AF, Vermerris W, Dolstra O, Visser RG, Trindade LM (2013) The potential of C4 grasses for cellulosic biofuel production. Front Plant Sci 4:107PubMedCentralPubMedGoogle Scholar
  92. Vicentini A, Barber JC, Aliscioni SS, Giussani LM, Kellogg EA (2008) The age of the grasses and clusters of origins of C4 photosynthesis. Glob Change Biol 14(12):2963–2977Google Scholar
  93. Vogan PJ, Sage RF (2012) Effects of low atmospheric CO2 and elevated temperature during growth on the gas exchange responses of C3, C3–C4 intermediate, and C4 species from three evolutionary lineages of C4 photosynthesis. Oecologia 169(2):341–352PubMedGoogle Scholar
  94. Vollbrecht E, Duvick J, Schares JP, Ahern KR, Deewatthanawong P, Xu L, Conrad LJ, Kikuchi K, Kubinec TA, Hall BD, Weeks R, Unger-Wallace E, Muszynski M, Brendel VP, Brutnell TP (2010) Genome-wide distribution of transposed Dissociation elements in maize. Plant Cell 22(6):1667–1685PubMedCentralPubMedGoogle Scholar
  95. 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(2):747–755Google Scholar
  96. Wang L, Peterson RB, Brutnell TP (2011) Regulatory mechanisms underlying C4 photosynthesis. New Phytol 190(1):9–20PubMedGoogle Scholar
  97. Westhoff P, Gowik U (2004) Evolution of C4 phosphoenolpyruvate carboxylase. Genes and proteins: a case study with the genus Flaveria. Ann Bot 93(1):13–23PubMedGoogle Scholar
  98. Westhoff P, Gowik U (2010) Evolution of C4 photosynthesis–looking for the master switch. Plant Physiol 154(2):598–601PubMedCentralPubMedGoogle Scholar
  99. Westhoff P, Offermann-Steinhard K, Höfer M, Eskins K, Oswald A, Streubel M (1991) Differential accumulation of plastidic transcripts encoding photosystem II components in the mesophyll and bundle sheath cells of monocotylednonous NADP-malic enzyme-type C4 plants. Planta 184:377–388PubMedGoogle Scholar
  100. Williams-Carrier R, Stiffler N, Belcher S, Kroeger T, Stern DB, Monde RA, Coalter R, Barkan A (2010) Use of Illumina sequencing to identify transposon insertions underlying mutant phenotypes in high-copy Mutator lines of maize. Plant J 63(1):167–177PubMedGoogle Scholar
  101. Wiludda C, Schulze S, Gowik U, Engelmann S, Koczor M, Streubel M, Bauwe H, Westhoff P (2012) Regulation of the photorespiratory GLDPA gene in C4 Flaveria: an intricate interplay of transcriptional and posttranscriptional processes. Plant Cell 24(1):137–151PubMedCentralPubMedGoogle Scholar
  102. Wyrich R, Dressen U, Brockmann S, Streubel M, Chang C, Qiang D, Paterson AH, Westhoff P (1998) The molecular basis of C4 photosynthesis in sorghum: isolation, characterization and RFLP mapping of mesophyll- and bundle-sheath-specific cDNAs obtained by differential screening. Plant Mol Biol 37(2):319–335PubMedGoogle Scholar
  103. Xin Z, Wang ML, Barkley NA, Burow G, Franks C, Pederson G, Burke J (2008) Applying genotyping (TILLING) and phenotyping analyses to elucidate gene function in a chemically induced sorghum mutant population. BMC Plant Biol 8:103PubMedCentralPubMedGoogle Scholar
  104. Zhang J, Peterson T (2005) A segmental deletion series generated by sister-chromatid transposition of Ac transposable elements in maize. Genetics 171(1):333–344PubMedGoogle Scholar
  105. Zhang G, Liu X, Quan Z, Cheng S, Xu X, Pan S, Xie M, Zeng P, Yue Z, Wang W, Tao Y, Bian C, Han C, Xia Q, Peng X, Cao R, Yang X, Zhan D, Hu J, Zhang Y, Li H, Li H, Li N, Wang J, Wang C, Wang R, Guo T, Cai Y, Liu C, Xiang H, Shi Q, Huang P, Chen Q, Li Y, Wang J, Zhao Z, Wang J (2012) Genome sequence of foxtail millet (Setaria italica) provides insights into grass evolution and biofuel potential. Nat Biotechnol 30(6):549–554PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Sarah Covshoff
    • 1
  • Steven J. Burgess
    • 1
  • Jana Kneřová
    • 1
  • Britta M. C. Kümpers
    • 1
  1. 1.Department of Plant SciencesUniversity of CambridgeCambridgeUK

Personalised recommendations