Skip to main content

Comparative Genomic Analysis of C4 Photosynthesis Pathway Evolution in Grasses

  • Chapter
  • First Online:
Genomics of the Saccharinae

Part of the book series: Plant Genetics and Genomics: Crops and Models ((PGG,volume 11))

Abstract

C4 plants are among the most productive crops, in part due to the efficiency at which their distinctive photosynthetic pathway fixes carbon at high temperatures. Sorghum and maize are C4 plants with full genome sequences available, facilitating a whole-genome level exploration of C4 pathway formation by comparing their respective versions of these key photosynthetic enzyme genes to those in the C3 plants rice and Brachypodium. A reservoir of duplicated genes was previously hypothesized to be a prerequisite for the evolution of C4 photosynthesis from a C3 progenitor. Grasses have been affected both by a whole-genome duplication (WGD) and individual gene duplications, and we show each of these mechanisms to have contributed to evolution of C4 photosynthesis. Some C4 genes appear to have been recruited directly from WGD duplicates followed by neofunctionalization. Others, such as the sorghum and maize carbonic anhydrase (CA) genes, have been recursively affected by tandem duplication, and mutations in stop codons have produced distinct C4 CA genes having 1–3 functional units, implying an interesting type of new gene formation accompanied by adaptive evolution. Key C4 enzymes in sorghum and maize show evidence of adaptive evolution, though differing in the level and mode. Intriguingly, a phosphoenolpyruvate carboxylase (PEPC) gene has also been evolving rapidly in both rice and Brachypodium and shows evidence of adaptive evolution, though lacking key mutations that are characteristic of C4 genes. The heterogeneity of origins of C4 genes suggests that there may have been a long transition process before the eventual establishment of C4 photosynthesis.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 229.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Aharoni A, Gaidukov L, Khersonsky O, McQ GS, Roodveldt C, Tawfik DS (2005) The ‘evolvability’ of promiscuous protein functions. Nat Genet 37:73–76

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Blanc G, Wolfe KH (2004a) Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. Plant Cell 16:1679–1691

    PubMed  CAS  Google Scholar 

  • Blanc G, Wolfe KH (2004b) Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. Plant Cell 16:1667–1678

    PubMed  CAS  Google Scholar 

  • Bowers JE, Chapman BA, Rong J, Paterson AH (2003) Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 422:433–438

    PubMed  CAS  Google Scholar 

  • Brown RH, Hattersley PW (1989) Leaf anatomy of C(3)-C(4) species as related to evolution of C(4) photosynthesis. Plant Physiol 91:1543–1550

    PubMed  CAS  Google Scholar 

  • Burnell JN, Chastain CJ (2006) Cloning and expression of maize-leaf pyruvate, Pi dikinase regulatory protein gene. Biochem Biophys Res Commun 345:675–680

    PubMed  CAS  Google Scholar 

  • Carels N, Bernardi G (2000) Two classes of genes in plants. Genetics 154:1819–1825

    PubMed  CAS  Google Scholar 

  • Casati P, Drincovich MF, Edwards GE, Andreo CS (1999) Malate metabolism by NADP-malic enzyme in plant defense. Photosynth Res 61:99–105

    CAS  Google Scholar 

  • Cerling TE, Harris JM, MacFadden BJ, Leasey MG, Quade J, Eisenmann V, Ehleringer JR (1997) Global vegetation change through the Miocene/Pliocene boundary. Nature 389:153–158

    CAS  Google Scholar 

  • Chapman BA, Bowers JE, Feltus FA, Paterson AH (2006) Buffering crucial functions by paleologous duplicated genes may impart cyclicality to angiosperm genome duplication. Proc Natl Acad Sci U S A 103:2730–2735

    PubMed  CAS  Google Scholar 

  • Chopra J, Kaur N, Gupta AK (2002) A comparative developmental pattern of enzymes of carbon metabolism and pentose phosphate pathway in mungbean and lentil nodules. Acta Physiol Plant 24:67–72

    CAS  Google Scholar 

  • Christin PA, Salamin N, Savolainen V, Duvall MR, Besnard G (2007) C4 photosynthesis evolved in grasses via parallel adaptive genetic changes. Curr Biol 17:1241–1247

    PubMed  CAS  Google Scholar 

  • Christin PA, Besnard G, Samaritani E, Duvall MR, Hodkinson TR, Savolainen V, Salamin N (2008) Oligocene CO2 decline promoted C4 photosynthesis in grasses. Curr Biol 18:37–43

    PubMed  CAS  Google Scholar 

  • Cretin C, Keryer E, Tagu D, Lepiniec L, Vidal J, Gadal P (1990) Complete cDNA sequence of sorghum phosphoenolpyruvate carboxylase involved in C4 photosynthesis. Nucleic Acids Res 18:658

    PubMed  CAS  Google Scholar 

  • Cretin C, Santi S, Keryer E, Lepiniec L, Tagu D, Vidal J, Gadal P (1991) The phosphoenolpyruvate carboxylase gene family of Sorghum: promoter structures, amino acid sequences and expression of genes. Gene 99:87–94

    PubMed  CAS  Google Scholar 

  • De Bodt S, Maere S, Van de Peer Y (2005) Genome duplication and the origin of angiosperms. Trends Ecol Evol 20:591–597

    PubMed  Google Scholar 

  • Edwards GE, Ku MSB (1987) Biochemistry of C3-C4 intermediates. In: Hatch MD, Boardman NK (eds) The biochemistry of plants. Academic, London, pp 275–325

    Google Scholar 

  • Ehleringer JR, Bjorkman O (1978) A comparison of photosynthetic characteristics of encelia species possessing glabrous and pubescent leaves. Plant Physiol 62:185–190

    PubMed  CAS  Google Scholar 

  • Emanuelsson O, Nielsen H, von Heijne G (1999) ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci 8:978–984

    PubMed  CAS  Google Scholar 

  • Felsenstein J (1992) Phylogenies from restriction sites—a maximum-likelihood approach. Evolution 46:159–173

    Google Scholar 

  • Freeling M, Thomas BC (2006) Gene-balanced duplications, like tetraploidy, provide predictable drive to increase morphological complexity. Genome Res 16:805–814

    PubMed  CAS  Google Scholar 

  • Fukayama H, Tsuchida H, Agarie S, Nomura M, Onodera H, Ono K, Lee BH, Hirose S, Toki S, Ku MS, Makino A, Matsuoka M, Miyao M (2001) Significant accumulation of C(4)-specific pyruvate, orthophosphate dikinase in a C(3) plant, rice. Plant Physiol 127:1136–1146

    PubMed  CAS  Google Scholar 

  • Gehring HH, Heute V, Kluge M (1998) Toward a better knowledge of the molecular evolution of phosphoenolpyruvate carboxylase by comparison of partial cDNA sequences. J Mol Evol 46:107–114

    Google Scholar 

  • Giussani LM, Cota-Sanchez JH, Zuloaga FO, Kellogg EA (2001) A molecular phylogeny of the grass subfamily Panicoideae (Poaceae) shows multiple origins of C4 photosynthesis. Am J Bot 88:1993–2012

    PubMed  CAS  Google Scholar 

  • Glackin CA, Grula JW (1990) Organ-specific transcripts of different size and abundance derive from the same pyruvate, orthophosphate dikinase gene in maize. Proc Natl Acad Sci U S A 87:3004–3008

    PubMed  CAS  Google Scholar 

  • Guindon S, Lethiec F, Duroux P, Gascuel O (2005) PHYML Online—a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Res 33:W557–W559

    PubMed  CAS  Google Scholar 

  • Haldane JBS (1932) The causes of evolution. Cornell University Press, Ithaca

    Google Scholar 

  • Hatch MD, Slack CR (1966) Photosynthesis by sugar-cane leaves. A new carboxylation reaction and the pathway of sugar formation. Biochem J 101:103–111

    PubMed  CAS  Google Scholar 

  • Hattersley PG (1983) The distribution of C3 and C4 grasses in Australia in relation to climate. Oecologia 57:113–128

    Google Scholar 

  • He X, Zhang J (2005a) Gene complexity and gene duplicability. Curr Biol 15:1016–1021

    PubMed  CAS  Google Scholar 

  • He XL, Zhang JZ (2005b) Rapid subfunctionalization accompanied by prolonged and substantial neofunctionalization in duplicate gene evolution. Genetics 169:1157–1164

    PubMed  Google Scholar 

  • Hibberd JM, Quick WP (2002) Characteristics of C4 photosynthesis in stems and petioles of C3 flowering plants. Nature 415:451–454

    PubMed  CAS  Google Scholar 

  • International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793–800

    Google Scholar 

  • Jaillon O, Aury JM, Noel B, Policriti A, Clepet C, Casagrande A, Choisne N, Aubourg S, Vitulo N, Jubin C, Vezzi A, Legeai F, Hugueney P, Dasilva C, Horner D, Mica E, Jublot D, Poulain J, Bruyere C, Billault A, Segurens B, Gouyvenoux M, Ugarte E, Cattonaro F, Anthouard V, Vico V, Del Fabbro C, Alaux M, Di Gaspero G, Dumas V, Felice N, Paillard S, Juman I, Moroldo M, Scalabrin S, Canaguier A, Le Clainche I, Malacrida G, Durand E, Pesole G, Laucou V, Chatelet P, Merdinoglu D, Delledonne M, Pezzotti M, Lecharny A, Scarpelli C, Artiguenave F, Pe ME, Valle G, Morgante M, Caboche M, Adam-Blondon AF, Weissenbach J, Quetier F, Wincker P (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–467

    PubMed  CAS  Google Scholar 

  • Kafri R, Dahan O, Levy J, Pilpel Y (2008) Preferential protection of protein interaction network hubs in yeast: evolved functionality of genetic redundancy. Proc Natl Acad Sci U S A 105:1243–1248

    PubMed  CAS  Google Scholar 

  • Kawamura T, Shigesada K, Toh H, Okumura S, Yanagisawa S, Izui K (1992) Molecular evolution of phosphoenolpyruvate carboxylase for C4 photosynthesis in maize: comparison of its cDNA sequence with a newly isolated cDNA encoding an isozyme involved in the anaplerotic function. J Biochem 112:147–154

    PubMed  CAS  Google Scholar 

  • Ku MS, Kano-Murakami Y, Matsuoka M (1996) Evolution and expression of C4 photosynthesis genes. Plant Physiol 111:949–957

    PubMed  CAS  Google Scholar 

  • Ku MS, Agarie S, Nomura M, Fukayama H, Tsuchida H, Ono K, Hirose S, Toki S, Miyao M, Matsuoka M (1999) High-level expression of maize phosphoenolpyruvate carboxylase in transgenic rice plants. Nat Biotechnol 17:76–80

    PubMed  CAS  Google Scholar 

  • Lepiniec L, Keryer E, Philippe H, Gadal P, Cretin C (1993) Sorghum phosphoenolpyruvate carboxylase gene family: structure, function and molecular evolution. Plant Mol Biol 21:487–502

    PubMed  CAS  Google Scholar 

  • Liang H, Li WH (2007) Gene essentiality, gene duplicability and protein connectivity in human and mouse. Trends Genet 23:375–378

    PubMed  CAS  Google Scholar 

  • Luchetta P, Cretin C, Gadal P (1991) Organization and expression of the two homologous genes encoding the NADP-malate dehydrogenase in Sorghum vulgare leaves. Mol Gen Genet 228:473–481

    PubMed  CAS  Google Scholar 

  • Lynch M, Conery JS (2003) The evolutionary demography of duplicate genes. J Struct Funct Genomics 3:35–44

    PubMed  CAS  Google Scholar 

  • Maere S, De Bodt S, Raes J, Casneuf T, Van Montagu M, Kuiper M, Van de Peer Y (2005) Modeling gene and genome duplications in eukaryotes. Proc Natl Acad Sci U S A 102:5454–5459

    PubMed  CAS  Google Scholar 

  • Matsuoka M (1995) The gene for pyruvate, orthophosphate dikinase in C4 plants: structure, regulation and evolution. Plant Cell Physiol 36:937–943

    PubMed  CAS  Google Scholar 

  • Maurino VG, Saigo M, Andreo CS, Drincovich MF (2001) Non-photosynthetic ‘malic enzyme’ from maize: a constituvely expressed enzyme that responds to plant defence inducers. Plant Mol Biol 45:409–420

    PubMed  CAS  Google Scholar 

  • Meyer A, Van de Peer Y (2005) From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). Bioessays 27:937–945

    PubMed  CAS  Google Scholar 

  • Mitsuhashi S, Mizushima T, Yamashita E, Yamamoto M, Kumasaka T, Moriyama H, Ueki T, Miyachi S, Tsukihara T (2000) X-ray structure of beta-carbonic anhydrase from the red alga, Porphyridium purpureum, reveals a novel catalytic site for CO(2) hydration. J Biol Chem 275:5521–5526

    PubMed  CAS  Google Scholar 

  • Miyao M (2003) Molecular evolution and genetic engineering of C4 photosynthetic enzymes. J Exp Bot 54:179–189

    PubMed  CAS  Google Scholar 

  • Monson RK (2003) Gene duplication, neofunctionalization, and the evolution of C4 photosynthesis. Int J Plant Sci 164:S43–S54

    CAS  Google Scholar 

  • Moroney JV, Bartlett SG, Samuelsson G (2001) Carbonic anhydrases in plants and algae. Plant Cell Environ 24:13

    Google Scholar 

  • Mulhaidat R, Sage RF, Dengler NG (2007) Diversity of kranz anatomy and biochemistry in C4 eudicots. Am J Bot 94:20

    Google Scholar 

  • Nielsen R, Bustamante C, Clark AG, Glanowski S, Sackton TB, Hubisz MJ, Fledel-Alon A, Tanenbaum DM, Civello D, White TJ, Sninsky JJ, Adams MD, Cargill M (2005) A scan for positively selected genes in the genomes of humans and chimpanzees. PLoS Biol 3:e170

    PubMed  Google Scholar 

  • Ohno S (1967) Sex chromosomes and sex-linked genes. Springler-Verlag, Berlin

    Google Scholar 

  • Ohno S (1970) Evolution by gene duplication. Springer, Berlin

    Google Scholar 

  • Papp B, Pal C, Hurst LD (2003) Dosage sensitivity and the evolution of gene families in yeast. Nature 424:194–197

    PubMed  CAS  Google Scholar 

  • Paterson AH, Bowers JE, Chapman BA (2004) Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics. Proc Natl Acad Sci U S A 101:9903–9908

    PubMed  CAS  Google Scholar 

  • Paterson AH, Chapman BA, Kissinger JC, Bowers JE, Feltus FA, Estill JC (2006) Many gene and domain families have convergent fates following independent whole-genome duplication events in Arabidopsis, Oryza, Saccharomyces and Tetraodon. Trends Genet 22:597–602

    PubMed  CAS  Google Scholar 

  • 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 R, Ware D, Westhoff P, Mayer KF, Messing J, Rokhsar DS (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457:551–556

    PubMed  CAS  Google Scholar 

  • Poetsch W, Hermans J, Westhoff P (1991) Multiple cDNAs of phosphoenolpyruvate carboxylase in the C4 dicot Flaveria trinervia. FEBS Lett 292:133–136

    PubMed  CAS  Google Scholar 

  • Pyankov VI, Artyusheva EG, Edwards GE, Black CC Jr, Soltis PS (2001) Phylogenetic analysis of tribe Salsoleae (Chenopodiaceae) based on ribosomal ITS sequences: implications for the evolution of photosynthesis types. Am J Bot 88:1189–1198

    PubMed  CAS  Google Scholar 

  • Rawsthorne S (1992) Towards an understanding of C3-C4 photosynthesis. Essays Biochem 27:135–146

    PubMed  CAS  Google Scholar 

  • Rondeau P, Rouch C, Besnard G (2005) NADP-malate dehydrogenase gene evolution in Andropogoneae (Poaceae): gene duplication followed by sub-functionalization. Ann Bot (Lond) 96:1307–1314

    CAS  Google Scholar 

  • Roth C, Liberles DA (2006) A systematic search for positive selection in higher plants (Embryophytes). BMC Plant Biol 6:12

    PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Salse J, Bolot S, Throude M, Jouffe V, Piegu B, Quraishi UM, Calcagno T, Cooke R, Delseny M, Feuillet C (2008) Identification and characterization of shared duplications between rice and wheat provide new insight into grass genome evolution. Plant Cell 20:11–24

    PubMed  CAS  Google Scholar 

  • Sanchez R, Cejudo FJ (2003) Identification and expression analysis of a gene encoding a bacterial-type phosphoenolpyruvate carboxylase from Arabidopsis and rice. Plant Physiol 132:949–957

    PubMed  CAS  Google Scholar 

  • 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 (New York, NY) 326:1112–1115

    CAS  Google Scholar 

  • Seemann JR, Sharkey TD, Wang J, Osmond CB (1987) Environmental effects on photosynthesis, nitrogen-use efficiency, and metabolite pools in leaves of sun and shade plants. Plant Physiol 84:796–802

    PubMed  CAS  Google Scholar 

  • Seoighe C, Gehring C (2004) Genome duplication led to highly selective expansion of the Arabidopsis thaliana proteome. Trends Genet 20:461–464

    PubMed  CAS  Google Scholar 

  • Shantz HL (1954) The place of grasslands in the earth’s cover of vegetation. Ecology 35:143–145

    Google Scholar 

  • Sheehy JE, Mitchell PL, Hardy B (2008) Charting new pathways To C4 rice. World Scientific, Los Banos, Philippines

    Google Scholar 

  • Sheen J (1991) Molecular mechanisms underlying the differential expression of maize pyruvate, orthophosphate dikinase genes. Plant Cell 3:225–245

    PubMed  CAS  Google Scholar 

  • Sheen J (1999) C4 gene expression. Annu Rev Plant Physiol Plant Mol Biol 50:187–217

    PubMed  CAS  Google Scholar 

  • Shenton M, Fontaine V, Hartwell J, Marsh JT, Jenkins GI, Nimmo HG (2006) Distinct patterns of control and expression amongst members of the PEP carboxylase kinase gene family in C4 plants. Plant J 48:45–53

    PubMed  CAS  Google Scholar 

  • Shi X, Wang X, Li Z, Zhu Q, Yang J, Ge S, Luo J (2007) Evidence that natural selection is the primary cause of the GC content variation in rice genes. J Integr Plant Biol 49:1393–1399

    CAS  Google Scholar 

  • Soltis PS (2005) Ancient and recent polyploidy in angiosperms. New Phytol 166:5–8

    PubMed  Google Scholar 

  • Sonnhammer ELL, Durbin R (1995) A dot-matrix program with dynamic threshold control suitable for genomic DNA and protein sequence analysis. Gene 167:1–10

    Google Scholar 

  • Steinke D, Hoegg S, Brinkmann H, Meyer A (2006) Three rounds (1R/2R/3R) of genome duplications and the evolution of the glycolytic pathway in vertebrates. BMC Biol 4:16

    PubMed  Google Scholar 

  • Svensson P, Blasing OE, Westhoff P (2003) Evolution of C4 phosphoenolpyruvate carboxylase. Arch Biochem Biophys 414:180–188

    PubMed  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    PubMed  CAS  Google Scholar 

  • Tang H, Bowers JE, Wang X, Ming R, Alam M, Paterson AH (2008a) Synteny and collinearity in plant genomes. Science (New York, NY) 320:486–488

    CAS  Google Scholar 

  • Tang HB, Wang XY, Bowers JE, Ming R, Alam M, Paterson AH (2008b) Unreveling ancient hexaploidy throught multiply-aligned angiosperm gene maps. Genome Res 18:1944–1954

    PubMed  CAS  Google Scholar 

  • Tang H, Bowers JE, Wang X, Paterson AH (2010) Angiosperm genome comparisons reveal early polyploidy in the monocot lineage. Proc Natl Acad Sci U S A 107:472–477

    PubMed  CAS  Google Scholar 

  • Taniguchi Y, Ohkawa H, Masumoto C, Fukuda T, Tamai T, Lee K, Sudoh S, Tsuchida H, Sasaki H, Fukayama H, Miyao M (2008) Overproduction of C4 photosynthetic enzymes in transgenic rice plants: an approach to introduce the C4-like photosynthetic pathway into rice. J Exp Bot 59:1799–1809

    PubMed  CAS  Google Scholar 

  • International Brachypodium Initiative (2010) Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature 463:763–768

    Google Scholar 

  • Tiwari A, Kumar P, Singh S, Ansari S (2005) Carbonic anhydrase in relation to higher plants. Photosynthetica 43:1–11

    CAS  Google Scholar 

  • Vicentini A, Barber JC, Aliscioni SS, Ciussani LM, Kellogg EA (2008) The age of the grasses and clusters of origins of C4 photosynthesis. Glob Chang Biol 14:15

    Google Scholar 

  • Wagner A (1997) A computational genomics approach to the identification of gene networks. Nucleic Acids Res 25:3594–3604

    PubMed  CAS  Google Scholar 

  • Wagner A (2007) Rapid detection of positive selection in genes and genomes through variation clusters. Genetics 176:2451–2463

    PubMed  CAS  Google Scholar 

  • Wang HC, Singer GA, Hickey DA (2004) Mutational bias affects protein evolution in flowering plants. Mol Biol Evol 21:90–96

    PubMed  Google Scholar 

  • Wang X, Shi X, Hao B, Ge S, Luo J (2005) Duplication and DNA segmental loss in the rice genome: implications for diploidization. New Phytol 165:937–946

    PubMed  CAS  Google Scholar 

  • Wang X, Shi X, Li Z, Zhu Q, Kong L, Tang W, Ge S, Luo J (2006) Statistical inference of ­chromosomal homology based on gene colinearity and applications to Arabidopsis and rice. BMC Bioinformatics 7:447

    PubMed  Google Scholar 

  • Wang X, Gowik U, Tang H, Bowers JE, Westhoff P, Paterson AH (2009) Comparative genomic analysis of C4 photosynthetic pathway evolution in grasses. Genome Biol 10:R68

    PubMed  Google Scholar 

  • Westhoff P, Gowik U (2004) Evolution of c4 phosphoenolpyruvate carboxylase. Genes and proteins: a case study with the genus Flaveria. Ann Bot (Lond) 93:13–23

    CAS  Google Scholar 

  • Wolfe KH, Li WH (2003) Molecular evolution meets the genomics revolution. Nat Genet 33(Suppl):255–265

    PubMed  CAS  Google Scholar 

  • Wong GK, Wang J, Tao L, Tan J, Zhang J, Passey DA, Yu J (2002) Compositional gradients in Gramineae genes. Genome Res 12:851–856

    PubMed  CAS  Google Scholar 

  • 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 37:319–335

    PubMed  CAS  Google Scholar 

  • Yang Z (1998) Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol Biol Evol 15:568–573

    PubMed  CAS  Google Scholar 

  • Yang Z, Nielsen R (1998) Synonymous and nonsynonymous rate variation in nuclear genes of mammals. J Mol Evol 46:409–418

    PubMed  CAS  Google Scholar 

  • Yu J, Wang J, Lin W, Li S, Li H, Zhou J, Ni P, Dong W, Hu S, Zeng C, Zhang J, Zhang Y, Li R, Xu Z, Li S, Li X, Zheng H, Cong L, Lin L, Yin J, Geng J, Li G, Shi J, Liu J, Lv H, Li J, Wang J, Deng Y, Ran L, Shi X, Wang X, Wu Q, Li C, Ren X, Wang J, Wang X, Li D, Liu D, Zhang X, Ji Z, Zhao W, Sun Y, Zhang Z, Bao J, Han Y, Dong L, Ji J, Chen P, Wu S, Liu J, Xiao Y, Bu D, Tan J, Yang L, Ye C, Zhang J, Xu J, Zhou Y, Yu Y, Zhang B, Zhuang S, Wei H, Liu B, Lei M, Yu H, Li Y, Xu H, Wei S, He X, Fang L, Zhang Z, Zhang Y, Huang X, Su Z, Tong W, Li J, Tong Z, Li S, Ye J, Wang L, Fang L, Lei T, Chen C, Chen H, Xu Z, Li H, Huang H, Zhang F, Xu H, Li N, Zhao C, Li S, Dong L, Huang Y, Li L, Xi Y, Qi Q, Li W, Zhang B, Hu W, Zhang Y, Tian X, Jiao Y, Liang X, Jin J, Gao L, Zheng W, Hao B, Liu S, Wang W, Yuan L, Cao M, McDermott J, Samudrala R, Wang J, Wong GK-S, Yang H (2005a) The genomes of Oryza sativa: a history of duplications. PLoS Biol 3:e38

    PubMed  Google Scholar 

  • Yu J, Wang J, Lin W, Li SG, Li H, Zhou J, Ni PX, Dong W, Hu SN, Zeng CQ, Zhang JG, Zhang Y, Li RQ, Xu ZY, Li ST, Li XR, Zheng HK, Cong LJ, Lin L, Yin JN, Geng JN, Li GY, Shi JP, Liu J, Lv H, Li J, Deng YJ, Ran LH, Shi XL, Wang XY, Wu QF, Li CF, Ren XY, Wang JQ, Wang XL, Li DW, Liu DY, Zhang XW, Ji ZD, Zhao WM, Sun YQ, Zhang ZP, Bao JY, Han YJ, Dong LL, Ji J, Chen P, Wu SM, Liu JS, Xiao Y, Bu DB, Tan JL, Yang L, Ye C, Zhang JF, Xu JY, Zhou Y, Yu YP, Zhang B, Zhuang SL, Wei HB, Liu B, Lei M, Yu H, Li YZ, Xu H, Wei SL, He XM, Fang LJ, Zhang ZJ, Zhang YZ, Huang XG, Su ZX, Tong W, Li JH, Tong ZZ, Li SL, Ye J, Wang LS, Fang L, Lei TT, Chen C, Chen H, Xu Z, Li HH, Huang HY, Zhang F, Xu HY, Li N, Zhao CF, Dong LJ, Huang YQ, Li L, Xi Y, Qi QH, Li WJ, Hu W, Zhang YL, Tian XJ, Jiao YZ, Liang XH, Jin JA, Gao L, Zheng WM, Hao BL, Liu SQ, Wang W, Yuan LP, Cao ML, McDermott J, Samudrala R, Wong GKS, Yang HM (2005b) The genomes of Oryza sativa: a history of duplications. PLoS Biol 3:266–281

    CAS  Google Scholar 

Download references

Acknowledgements

We appreciate financial support from the US National Science Foundation (MCB-0450260), CGIAR Generation Challenge Program, and United Sorghum Checkoff Program.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xiyin Wang .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer Science+Business Media New York

About this chapter

Cite this chapter

Wang, X., Paterson, A.H. (2013). Comparative Genomic Analysis of C4 Photosynthesis Pathway Evolution in Grasses. In: Paterson, A. (eds) Genomics of the Saccharinae. Plant Genetics and Genomics: Crops and Models, vol 11. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-5947-8_19

Download citation

Publish with us

Policies and ethics