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Major alterations in transcript profiles between C3–C4 and C4 photosynthesis of an amphibious species Eleocharis baldwinii

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Abstract

Engineering C4 photosynthetic metabolism into C3 crops is regarded as a major strategy to increase crop productivity, and clarification of the evolutionary processes of C4 photosynthesis can help the better use of this strategy. Here, Eleocharis baldwinii, a species in which C4 photosynthesis can be induced from a C3 –C4 state under either environmental or ABA treatments, was used to identify the major transcriptional modifications during the process from C3 –C4 to C4. The transcriptomic comparison suggested that in addition to the major differences in C4 core pathway, the pathways of glycolysis, citrate acid metabolism and protein synthesis were dramatically modified during the inducement of C4 photosynthetic states. Transcripts of many transporters, including not only metabolite transporters but also ion transporters, were dramatically increased in C4 photosynthetic state. Many candidate regulatory genes with unidentified functions were differentially expressed in C3 –C4 and C4 photosynthetic states. Finally, it was indicated that ABA, auxin signaling and DNA methylation play critical roles in the regulation of C4 photosynthesis. In summary, by studying the different photosynthetic states of the same species, this work provides the major transcriptional differences between C3 –C4 and C4 photosynthesis, and many of the transcriptional differences are potentially related to C4 development and therefore are the potential targets for reverse genetics studies.

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References

  • Aloni R, Schwalm K, Langhans M, Ullrich CI (2003) Gradual shifts in sites of free-auxin production during leaf-primordium development and their role in vascular differentiation and leaf morphogenesis in Arabidopsis. Planta 216(5):841–853

    CAS  PubMed  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215(3):403–410

    Article  CAS  PubMed  Google Scholar 

  • Ariel FD, Manavella PA, Dezar CA, Chan RL (2007) The true story of the HD-Zip family. Trends Plant Sci 12(9):419–426

    Article  CAS  PubMed  Google Scholar 

  • Bartley GE, Scolnik PA (1995) Plant carotenoids: pigments for photoprotection, visual attraction, and human health. Plant Cell 7(7):1027–1038

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 1165–1188

  • Bolle C, Koncz C, Chua NH (2000) PAT1, a new member of the GRAS family, is involved in phytochrome A signal transduction. Genes Dev 14(10):1269–1278

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bossi F, Cordoba E, Dupre P, Mendoza MS, Roman CS, Leon P (2009) The Arabidopsis ABA-iNSENSITIVE (ABI) 4 factor acts as a central transcription activator of the expression of its own gene, and for the induction of ABI5 and SBE2. 2 genes during sugar signaling. The. Plant J 59(3):359–374

    Article  CAS  PubMed  Google Scholar 

  • Botha CEJ (1992) Plasmodesmatal distribution, structure and frequency in relation to assimilation in C3 and C4 grasses in southern Africa. Planta 187(3):348–358

    CAS  PubMed  Google Scholar 

  • Brautigam A, Hofmann-Benning S, Weber AP (2008) Comparative proteomics of chloroplasts envelopes from C3 and C4 plants reveals specific adaptations of the plastid envelope to C4 photosynthesis and candidate proteins required for maintaining C4 metabolite fluxes. Plant Physiol 148:568–579

    Article  PubMed Central  PubMed  Google Scholar 

  • Brautigam 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 155:142–156

    Article  PubMed Central  PubMed  Google Scholar 

  • Brown NJ, Parsley K, Hibberd JM (2005) The future of C4 research—Maize, Flaveria or Cleome? Trends Plant Sci 10(5):215–221

    Article  CAS  PubMed  Google Scholar 

  • 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 22:2537–2544

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chen T, Ye R, Fan X, Li X, Lin Y (2011) Identification of C4 photosynthesis metabolism and regulatory associated genes in Eleocharis vivipara by SSH. Photosynth Res 108:157–170

    Article  CAS  PubMed  Google Scholar 

  • Cheong YH, Pandey GK, Grant JJ, Batistic O, Li L, Kim BG, Lee SC, Kudla J, Luan S (2007) Two calcineurin B-like calcium sensors, interacting with protein kinase CIPK23, regulate leaf transpiration and root potassium uptake in Arabidopsis. The Plant J 52(2):223–239

    Article  CAS  Google Scholar 

  • Chinnusamy V, Zhu JK (2009) Epigenetic regulation of stress responses in plants. Curr Opin Plant Biol 12(2):133–139

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Choi H, Hong J, Ha J, Kang J, Kim SY (2000) ABFs, a family of ABA-responsive element binding factors. J Biol Chem 275(3):1723–1730

    Article  CAS  PubMed  Google Scholar 

  • Choi HI, Park HJ, Park JH, Kim S, Im MY, Seo HH, Kim YW, Hwang I, Kim SY (2005) Arabidopsis calcium-dependent protein kinase AtCPK32 interacts with ABF4, a transcriptional regulator of abscisic acid-responsive gene expression, and modulates its activity. Plant Physiol 139(4):1750–1761

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Clark SE, Williams RW, Meyerowitz EM (1997) The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 89(4):575–585

    Article  CAS  PubMed  Google Scholar 

  • 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):1469–1481

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a Core signaling network. Ann Rev Plant Biol 61:26.21–26.29

  • Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible WR (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol 139(1):5–17

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dai M, Hu Y, Zhao Y, Liu H, Zhou DX (2007) A WUSCHEL-LIKE HOMEOBOX gene represses a YABBY gene expression required for rice leaf development. Plant Physiol 144(1):380–390

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dellaporta SL, Wood J, Hicks JB (1983) A plant DNA minipreparation: version II. Plant Mol Biol Rep 1(4):19–21

    Article  CAS  Google Scholar 

  • Di Laurenzio L, Wysocka-Diller J, Malamy JE, Pysh L, Helariutta Y, Freshour G, Hahn MG, Feldmann KA, Benfey PN (1996) The SCARECROW gene regulates an asymmetric cell division that is essential for generating the radial organization of the arabidopsis root. Cell 86(3):423–433

    Article  PubMed  Google Scholar 

  • Evert RF, Eschrich W, Heyser W (1977) Distribution and structure of the plasmodesmata in mesophyll and bundle-sheath cells of Zea mays L. Planta 136(1):77–89

    Article  CAS  PubMed  Google Scholar 

  • 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):1219–1250

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Furbank RT, Hatch MD (1987) Mechanism of C4 photosynthesis: the size and composition of the inorganic carbon pool in bundle sheath cells. Plant Physiol 85(4):958–964

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gaedeke N, Klein M, Kolukisaoglu U, Forestier C, Muller A, Ansorge M, Becker D, Mamnun Y, Kuchler K, Schulz B, Mueller-Roeber B, Martinoia E (2001) The Arabidopsis thaliana ABC transporter AtMRP5 controls root development and stomata movement. EMBO J 20(8):1875–1887

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gowik U, Brautigam 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 23:2087–2105

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hale GM, Querry MR (1973) Optical constants of water in the 200-nm to 200-microm wavelength region. Appl Opt 12(3):555–563

    Article  CAS  PubMed  Google Scholar 

  • Häusler RE, Rademacher T, Li J, Lipka V, Fischer KL, Schubert S, Kreuzaler F, Hirsch HJ (2001) Single and double overexpression of C4-cycle genes had differential effects on the pattern of endogenous enzymes, attenuation of photorespiration and on contents of UV protectants in transgenic potato and tobacco plants. J Exp Bot 52(362):1785–1803

    Article  PubMed  Google Scholar 

  • 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):228–231

    Article  CAS  PubMed  Google Scholar 

  • Hoecker U, Vasil IK, McCarty DR (1995) Integrated control of seed maturation and germination programs by activator and repressor functions of Viviparous-1 of maize. Genes Dev 9(20):2459–2469

    Article  CAS  PubMed  Google Scholar 

  • Horst I, Offermann S, Dreesen B, Niessen M, Pn C (2009) Core promoter acetylation is not required for high transcription from the phosphoenolpyruvate carboxylase promoter in maize. Epigenetics Chromatin 2:17

    Article  PubMed Central  PubMed  Google Scholar 

  • Kang J, Hwang JU, Lee M, Kim YY, Assmann SM, Martinoia E, Lee Y (2010) PDR-type ABC transporter mediates cellular uptake of the phytohormone abscisic acid. Proc Natl Acad Sci USA 107(5):2355–2360

  • Kato H, Motomura T, Komeda Y, Saito T, Kato A (2010) Overexpression of the NAC transcription factor family gene ANAC036 results in a dwarf phenotype in Arabidopsis thaliana. J Plant Physiol 167(7):571–577

    Article  CAS  PubMed  Google Scholar 

  • Kim C, Lee KP, Baruah A, Nater M, Gobel C, Feussner I, Apel K (2009) 1O2-mediated retrograde signaling during late embryogenesis predetermines plastid differentiation in seedlings by recruiting abscisic acid. Proc Natl Acad Sci USA 106(24):9920–9924

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Koiwa H, Barb AW, Xiong L, Li F, McCully MG, Lee BH, Sokolchik I, Zhu J, Gong Z, Reddy M, Sharkhuu A, Manabe Y, Yokoi S, Zhu JK, Bressan RA, Hasegawa PM (2002) C-terminal domain phosphatase-like family members (AtCPLs) differentially regulate Arabidopsis thaliana abiotic stress signaling, growth, and development. Proc Natl Acad Sci USA 99(16):10893–10898

  • Kubis S, Patel R, Combe J, Bedard J, Kovacheva S, Lilley K, Biehl A, Leister D, Rios G, Koncz C (2004) Functional specialization amongst the Arabidopsis Toc159 family of chloroplast protein import receptors. Plant Cell 16(8):2059–2077

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kuromori T, Shinozaki K (2010) ABA transport factors found in Arabidopsis ABC transporters. Plant Sig Beh 5(9):1124–1126

    Article  CAS  Google Scholar 

  • Langdale JA, Kidner CA (1994) Bundle sheath defective, a mutation that disrupts cellular differentiation in maize leaves. Development 120(3):673–681

    Google Scholar 

  • Leegood RC (2002) C4 photosynthesis: principles of CO2 concentration and prospects for its introduction into C3 plants. J Exp Bot 53(369):581–590

    Article  CAS  PubMed  Google Scholar 

  • Leivar P, Tepperman JM, Monte E, Calderon RH, Liu TL, Quail PH (2009) Definition of early transcriptional circuitry involved in light-induced reversal of PIF-imposed repression of photomorphogenesis in young Arabidopsis seedlings. Plant Cell 21(11):3535–3553

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Li R, Zhu H, Ruan J, Qian W, Fang X, Shi Z, Li Y, Li S, Shan G, Kristiansen K, Yang H, Wang J (2009) De novo assembly of human genomes with massively parallel short read sequencing. Genome Res 20(2):265–272

    Article  PubMed  Google Scholar 

  • 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 42:1060–1067

    Article  CAS  PubMed  Google Scholar 

  • Lu YP, Li ZS, Drozdowicz YM, Hortensteiner S, Martinoia E, Rea PA (1998) AtMRP2, an Arabidopsis ATP binding cassette transporter able to transport glutathione S-conjugates and chlorophyll catabolites: functional comparisons with Atmrp1. Plant Cell 10(2):267–282

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lunn JE, Furbank RT (1997) Localisation of sucrose-phosphate synthase and starch in leaves of C4 plants. Planta 202(1):106–111

    Article  CAS  PubMed  Google Scholar 

  • Maai E, Shimada S, Yamada M, Sugiyama T, Miyake H, Taniguchi M (2011) The avoidance and aggregative movements of mesophyll chloroplasts in C4 monocots in response to blue light and abscisic acid. J Exp Bot 62:3213–3221

    Article  CAS  PubMed  Google Scholar 

  • Majeran W, Zybailov B, Ytterberg AJ, Dunsmore J, Sun Q, van Wijk KJ (2008) Consequences of C4 differentiation for chloroplast membrane proteomes in maize mesophyll and bundle sheath cells. Mol Cell Proteomics 7(9):1609–1638

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 22:3509–3542

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Matsubayashi Y, Ogawa M, Kihara H, Niwa M, Sakagami Y (2006) Disruption and overexpression of Arabidopsis phytosulfokine receptor gene affects cellular longevity and potential for growth. Plant Physiol 142(1):45–53

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Matsuoka M, Furbank RT, Fukayama H, Miyao M (2001) Molecular Engineering of C4 Photosynthesis. Ann Rev Plant Physiol Plant Mol Biol 52:297–314

    CAS  Google Scholar 

  • Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621–628

    Article  CAS  PubMed  Google Scholar 

  • Nakamura H, Muramatsu M, Hakata M, Ueno O, Nagamura Y, Hirochika H, Takano M, Ichikawa H (2009) Ectopic overexpression of the transcription factor OsGLK1 induces chloroplast development in non-green rice cells. Plant Cell Physiol 50(11):1933–1949

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nambara E, Marion-Poll A (2005) Abscisic acid biosynthesis and catabolism. Ann Rev Plant Biol 56:165–185

    Article  CAS  Google Scholar 

  • Nelson T (2011) The grass leaf developmental gradient as a platform for a systems understanding of the anatomical specialization of C4 leaves. J Exp Bot 62:3039–3048

    Article  CAS  PubMed  Google Scholar 

  • Nelson T, Dengler N (1997) Leaf vascular pattern formation. Plant Cell 9(7):1121–1135

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nemhauser JL, Hong F, Chory J (2006) Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses. Cell 126(3):467–475

    Article  CAS  PubMed  Google Scholar 

  • Offermann S, Dreesen B, Horst I, Danker T, Jaskiewicz M, Peterhansel C (2008) Developmental and environmental signals induce distinct histone acetylation profiles on distal and proximal promoter elements of the C4-Pepc gene in maize. Genetics 179(4):1891–1901

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Oikawa K, Kasahara M, Kiyosue T, Kagawa T, Suetsugu N, Takahashi F, Kanegae T, Niwa Y, Kadota A, Wada M (2003) Chloroplast unusual positioning1 is essential for proper chloroplast positioning. Plant Cell 15(12):2805–2815

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Okushima Y, Mitina I, Quach HL, Theologis A (2005) AUXIN RESPONSE FACTOR 2 (ARF2): a pleiotropic developmental regulator. Plant J 43(1):29–46

    Article  CAS  PubMed  Google Scholar 

  • Oyama T, Shimura Y, Okada K (1997) The Arabidopsis HY5 gene encodes a bZIP protein that regulates stimulus-induced development of root and hypocotyl. Genes Dev 11(22):2983–2995

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pandey S, Chen JG, Jones AM, Assmann SM (2006) G-protein complex mutants are hypersensitive to abscisic acid regulation of germination and postgermination development. Plant Physiol 141(1):243–256

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Park J, Knoblauch M, Okita TW, Edwards GE (2009a) 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(2):369–382

    Article  CAS  PubMed  Google Scholar 

  • Park SY, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, Chow TF (2009b) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science’s STKE 324(5930):1068–1071

    CAS  Google Scholar 

  • Pighin JA, Zheng H, Balakshin LJ, Goodman IP, Western TL, Jetter R, Kunst L, Samuels AL (2004) Plant cuticular lipid export requires an ABC transporter. Science 306:702–704

    Article  CAS  PubMed  Google Scholar 

  • Plucken H, Muller B, Grohmann D, Westhoff P, Eichacker LA (2002) The HCF136 protein is essential for assembly of the photosystem II reaction center in Arabidopsis thaliana. FEBS Lett 532:85–90

    Article  CAS  PubMed  Google Scholar 

  • Ponting CP, Aravind L (1999) START: a lipid-binding domain in StAR, HD-ZIP and signalling proteins. Trends Biochem Sci 24(4):130–132

    Article  CAS  PubMed  Google Scholar 

  • Saez A, Rodrigues A, Santiago J, Rubio S, Rodriguez PL (2008) HAB1-SWI3B interaction reveals a link between abscisic acid signaling and putative SWI/SNF chromatin-remodeling complexes in Arabidopsis. Plant cell 20(11):2972–2988

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sage RF (2004) The evolution of C4 photosynthesis. New Phytol 161(2):341–370

    Article  CAS  Google Scholar 

  • Sage RF, Christin PA, Edwards EJ (2011) The C4 plant lineages of planet Earth. J Exp Bot 62:3039–3048

    Article  Google Scholar 

  • Sage RF, Sage TL, Kocacinar F (2012) Photorespiration and the evolution of C4 photosynthesis. Ann Rev Plant Biol 63:19–47

    Article  CAS  Google Scholar 

  • Shen YY, Wang XF, Wu FQ, Du SY, Cao Z, Shang Y, Wang XL, Peng CC, Yu XC, Zhu SY (2006) The Mg-chelatase H subunit is an abscisic acid receptor. Nature 443(7113):823–826

    Article  CAS  PubMed  Google Scholar 

  • Slewinski TL, Anderson AA, Zhang C, Turgeon R (2013) Scarecrow plays a role in establishing Kranz anatomy in maize leaves. Plant Cell Physiol 53(12):2030–2037

    Google Scholar 

  • Su PH, Li H (2008) Arabidopsis stromal 70-kD heat shock proteins are essential for plant development and important for thermotolerance of germinating seeds. Plant Physiol 146(3):1231–1241

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Surridge C (2002) Agricultural biotech: the rice squad. Nature 416(6881):576–578

    Article  CAS  PubMed  Google Scholar 

  • Terashima I, Hanba YT, Tazoe Y, Vyas P, Yano S (2006) Irradiance and phenotype: comparative eco-development of sun and shade leaves in relation to photosynthetic CO2 diffusion. J Exp Bot 57(2):343–354

    Article  CAS  PubMed  Google Scholar 

  • Tolley BJ, Woodfield H, Wanchana S, Bruskiewich R, Hibberd JM (2012) Light-regulated and cell-specific methylation of the maize PEPC promoter. J Exp Bot 63:1381–1390

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Uchino A, Samejima M, Ishii R, Ueno O (1995) Photosynthetic carbon metabolism in an amphibious sedge, Eleocharis baldwinii (Torr.) Chapman: modified expression of C4 characteristics under submerged aquatic conditions. Plant Cell Physiol 36(2):229–238

    CAS  Google Scholar 

  • Ueno O (1998) Induction of kranz anatomy and C4-like biochemical characteristics in a submerged amphibious plant by abscisic acid. Plant Cell 10(4):571–584

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ueno O (2004) Environmental regulation of photosynthetic metabolism in the amphibious sedge Eleocharis baldwinii and comparisons with related species. Plant, Eell Environ 27(5):627–639

    Article  CAS  Google Scholar 

  • 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):6733–6737

  • Uno Y, Furihata T, Abe H, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K (2000) Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc Natl Acad Sci USA 97(21):11632–11637

  • Usami T, Horiguchi G, Yano S, Tsukaya H (2009) The more and smaller cells mutants of Arabidopsis thaliana identify novel roles for SQUAMOSA PROMOTER BINDING PROTEIN-LIKE genes in the control of heteroblasty. Development 136(6):955–964

    Article  CAS  PubMed  Google Scholar 

  • Van Lijsebettens M, Grasser KD (2010) The role of the transcript elongation factors FACT and HUB1 in leaf growth and the induction of flowering. Plant Signal Behav 5(6):715–717

    Article  PubMed Central  PubMed  Google Scholar 

  • Vasil V, Marcotte WR Jr, Rosenkrans L, Cocciolone SM, Vasil IK, Quatrano RS, McCarty DR (1995) Overlap of Viviparous1 (VP1) and abscisic acid response elements in the Em promoter: G-box elements are sufficient but not necessary for VP1 transactivation. Plant Cell 7(9):1511–1518

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Von Caemmerer S, Furbank RT (2003) The C4 pathway: an efficient CO2 pump. Photosynth Res 77:191–207

    Article  Google Scholar 

  • von Kanel T, Gerber D, Schaller A, Baumer A, Wey E, Jackson CB, Gisler FM, Heinimann K, Gallati S (2010) Quantitative 1-step DNA methylation analysis with native genomic DNA as template. Clin Chem 56(7):1098–1106

    Article  Google Scholar 

  • Voznesenskaya E, Franceschi V, Kiirats O, Freitag H, Edwards G (2001) Kranz anatomy is not essential for terrestrial C4 plant photosynthesis. Nature 414(6863):543–546

    Article  CAS  PubMed  Google Scholar 

  • 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(5):649–662

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Xie W, Chen Y, Tang W, Yang J, Ye R, Liu L, Lin Y, Xu C, Xiao J, Zhang Q (2009) A dynamic gene expression atlas covering the entire life cycle of rice. Plant J 61(5):752–766

    Article  PubMed  Google Scholar 

  • Weber AP, von Caemmerer S (2010) Plastid transport and metabolism of C3 and C4 plants—comparative analysis and possible biotechnological exploitation. Curr Opin Plant Biol 13(3):257–265

    Article  CAS  PubMed  Google Scholar 

  • Whitney SM, Sharwood RE, Orr D, White SJ, Alonso H, Galmés J (2011) Isoleucine 309 acts as a C4 catalytic switch that increases ribulose-1, 5-bisphosphate carboxylase/oxygenase (rubisco) carboxylation rate in Flaveria. Proc Natl Acad Sci USA 108(35):14688–14693

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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(10):1736–1749

    CAS  PubMed  Google Scholar 

  • Zhu SY, Yu XC, Wang XJ, Zhao R, Li Y, Fan RC, Shang Y, Du SY, Wang XF, Wu FQ (2007) Two calcium-dependent protein kinases, CPK4 and CPK11, regulate abscisic acid signal transduction in Arabidopsis. Plant Cell 19(10):3019–3036

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhu XG, Long SP, Ort DR (2010) Improving photosynthetic efficiency for greater yield. Ann Rev Plant Biol 61:235–261

    Article  CAS  Google Scholar 

  • Zourelidou M, MUller I, Willige BC, Nill C, Jikumaru Y, Li H, Schwechheimer C (2009) The polarly localized D6 PROTEIN KINASE is required for efficient auxin transport in Arabidopsis thaliana. Development 136(4):627–636

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Acknowledgments

Sincerely thanks to all the anonymous referees for their patience and constructive comments. This research were supported by The National Natural Science Foundation of China, the National High Technology Research and Development Program of China (863 Program), the Ministry of Science and Technology 2011DFA31070, Shanghai Pujiang program Y057C11501, and the National Program on Research and Development of Transgenic Plants.

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  1. National Key Laboratory of Crop Genetic Improvement, National Centre of Plant Gene Research, Huazhong Agricultural University, Wuhan, 430070, China

    Taiyu Chen & Yongjun Lin

  2. College of Plant Science & Technology, Huazhong Agricultural University, Wuhan , 430070, China

    Taiyu Chen

  3. CAS Key Laboratory of Computational Biology, CAS-MPG Partner Institute for Computational Biology, Shanghai, 200031, China

    Xin-Guang Zhu

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Chen, T., Zhu, XG. & Lin, Y. Major alterations in transcript profiles between C3–C4 and C4 photosynthesis of an amphibious species Eleocharis baldwinii . Plant Mol Biol 86, 93–110 (2014). https://doi.org/10.1007/s11103-014-0215-8

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