Skip to main content

Advertisement

SpringerLink
Log in

Exploring natural variation of photosynthesis in a site-specific manner: evolution, progress, and prospects

  • Review
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

Site-specific changes of photosynthesis, a relatively new concept, can be used to improve the productivity of critical food crops to mitigate the foreseen food crisis.

Abstract

Global food security is threatened by an increasing population and the effects of climate change. Large yield improvements were achieved in major cereal crops between the 1950s and 1980s through the Green Revolution. However, we are currently experiencing a significant decline in yield progress. Of the many approaches to improved cereal yields, exploitation of the mode of photosynthesis has been intensely studied. Even though the C4 pathway is considered the most efficient, mainly because of the carbon concentrating mechanisms around the enzyme ribulose-1,5-bisphosphate carboxylase/oxygenase, which minimize photorespiration, much is still unknown about the specific gene regulation of this mode of photosynthesis. Most of the critical cereal crops, including wheat and rice, are categorized as C3 plants based on the photosynthesis of major photosynthetic organs. However, recent findings raise the possibility of different modes of photosynthesis occurring at different sites in the same plant and/or in plants grown in different habitats. That is, it seems possible that efficient photosynthetic traits may be expressed in specific organs, even though the major photosynthetic pathway is C3. Knowledge of site-specific differences in photosynthesis, coupled with site-specific regulation of gene expression, may therefore hold a potential to enhance the yields of economically important C3 crops.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alexandratos N, Bruinsma J (2012) World agriculture towards 2030/2050: the 2012 revision. ESA Working paper FAO, Rome

    Google Scholar 

  • Allen JF, Martin W (2007) Evolutionary biology: out of thin air. Nature 445:610

    Article  CAS  PubMed  Google Scholar 

  • Austin R, Ford MA, Morgan C (1989) Genetic improvement in the yield of winter wheat: a further evaluation. J Agric Sci 112:295–301

    Article  Google Scholar 

  • Bauwe H, Hagemann M, Fernie AR (2010) Photorespiration: players, partners and origin. Trends in plant science 15:330–336

    Article  CAS  PubMed  Google Scholar 

  • Beadle C, Long S (1985) Photosynthesis—is it limiting to biomass production? Biomass 8:119–168

    Article  CAS  Google Scholar 

  • Beerling DJ, Royer DL (2011) Convergent cenozoic CO2 history. Nat Geosci 4:418–420

    Article  CAS  Google Scholar 

  • Berardy A, Chester MV (2017) Climate change vulnerability in the food, energy, and water nexus: concerns for agricultural production in Arizona and its urban export supply. Environ Res Lett 12:035004

    Article  Google Scholar 

  • Black CC, Mollenhauer HH (1971) Structure and distribution of chloroplasts and other organelles in leaves with various rates of photosynthesis. Plant Physiol 47:15–23

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blankenship RE et al (2011) Comparing photosynthetic and photovoltaic efficiencies and recognizing the potential for improvement. Science 332:805–809

    Article  CAS  PubMed  Google Scholar 

  • Bouchenak-Khelladi Y, Anthony Verboom G, Hodkinson TR, Salamin N, Francois O, Ni Chonghaile G, Savolainen V (2009) The origins and diversification of C4 grasses and savanna-adapted ungulates. Glob Change Biol 15(10):2397–2417

    Article  Google Scholar 

  • Bowes G, Salvucci ME (1989) Plasticity in the photosynthetic carbon metabolism of submersed aquatic macrophytes. Aquat Bot 34:233–266

    Article  CAS  Google Scholar 

  • Bowes G, Ogren W, Hageman R (1971) Phosphoglycolate production catalyzed by ribulose diphosphate carboxylase. Biochem Biophys Res Commun 45:716–722

    Article  CAS  PubMed  Google Scholar 

  • Bräutigam A et al (2010) An mRNA blueprint for C4 photosynthesis derived from comparative transcriptomics of closely related C3 and C4 species. Plant Physiolpp. https://doi.org/10.1104/pp.110.159442

    Article  Google Scholar 

  • Brown NJ et al (2010) C4 acid decarboxylases required for C4 photosynthesis are active in the mid-vein of the C3 species Arabidopsis thaliana, and are important in sugar and amino acid metabolism. Plant J 61:122–133

    Article  CAS  PubMed  Google Scholar 

  • Burgess SJ, Hibberd JM (2015) Insights into C 4 metabolism from comparative deep sequencing. Curr Opin Plant Biol 25:138–144

    Article  CAS  PubMed  Google Scholar 

  • Busch FA, Farquhar GD (2016) Poor evidence for C4 photosynthesis in the wheat grain. Plant Physiol 172:1357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Busch FA, Sage TL, Cousins AB, Sage RF (2013) C3 plants enhance rates of photosynthesis by reassimilating photorespired and respired CO2 Plant. Cell Environ 36:200–212

    Article  CAS  Google Scholar 

  • Bykova NV, Keerberg O, Pärnik T, Bauwe H, Gardeström P (2005) Interaction between photorespiration and respiration in transgenic potato plants with antisense reduction in glycine decarboxylase. Planta 222:130–140

    Article  CAS  PubMed  Google Scholar 

  • Cai Z, Liu G, Zhang J, Li Y (2014) Development of an activity-directed selection system enabled significant improvement of the carboxylation efficiency of Rubisco. Protein Cell 5:552–562

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Campany CE, Medlyn BE, Duursma R (2017) Reduced growth due to belowground sink limitation is not fully explained by reduced photosynthesis. Tree Physiol 37:1042–1054

    Article  CAS  PubMed  Google Scholar 

  • Canfield DE (2005) The early history of atmospheric oxygen: homage to Robert M. Garrels Annu Rev Earth Planet Sci 33:1–36

    Article  CAS  Google Scholar 

  • Cano FJ, López R, Warren CR (2014) Implications of the mesophyll conductance to CO2 for photosynthesis and water-use efficiency during long-term water stress and recovery in two contrasting Eucalyptus species. Plant Cel Environ 37:2470–2490

    Article  CAS  Google Scholar 

  • Casati P, Lara MV, Andreo CS (2000) Induction of a C4-Like mechanism of co2 fixation in egeria densa, a submersed aquatic species. Plant Physiol 123:1611–1622

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Casler MD et al (2011) The switchgrass genome: tools and strategies The Plant. Genome 4:273–282

    CAS  Google Scholar 

  • Chen M, Blankenship RE (2011) Expanding the solar spectrum used by photosynthesis. Trends Plant Sci 16:427–431

    Article  CAS  PubMed  Google Scholar 

  • Christin PA, Osborne CP (2013) The recurrent assembly of C4 photosynthesis, an evolutionary tale. Photosynth Res 117:163–175

    Article  CAS  PubMed  Google Scholar 

  • Chuong SD, Franceschi VR, Edwards GE (2006) The cytoskeleton maintains organelle partitioning required for single-cell C4 photosynthesis in Chenopodiaceae species. Plant Cell 18:2207–2223

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clay J (2011) Freeze the footprint of food. Nature 475:287–289

    Article  CAS  PubMed  Google Scholar 

  • Crist E, Mora C, Engelman R (2017) The interaction of human population, food production, and biodiversity protection. Science 356:260–264

    Article  CAS  PubMed  Google Scholar 

  • Danila FR, Quick WP, White RG, Furbank RT, von Caemmerer S (2018) CORRECTION: The metabolite pathway between bundle sheath and mesophyll: quantification of plasmodesmata in leaves of C3 and C4 monocots. Plant Cell 30(2):tpc.00115.2018

    Google Scholar 

  • Dengler N, Nelson T (1999) Leaf structure and development in C4 plants. In: Sage RF, Monson RK (eds) C4 plant biology. Academic Press, San Diego

    Google Scholar 

  • Dengler NG, Dengler RE, Donnelly PM, Hattersley PW (1994) Quantitative leaf anatomy of C3 and C4 grasses (Poaceae): bundle sheath and mesophyll surface area relationships. Ann Bot 73:241–255

    Article  Google Scholar 

  • Duffus C, Rosie R (1973) Some enzyme activities associated with the chlorophyll containing layers of the immature barley pericarp. Planta 114:219–226

    Article  CAS  PubMed  Google Scholar 

  • Edwards GE, Ku MSB, Monson RK (1985) C4 photosynthesis and its regulation. In: Barber J, Baker NR (eds) Photosynthetic mechanisms and the environment. Elsevier Science, Amsterdam, pp 287–327

    Google Scholar 

  • Edwards GE, Franceschi VR, Voznesenskaya EV (2004) Single-cell C4 photosynthesis versus the dual-cell (Kranz) paradigm. Annu Rev Plant Biol 55:173–196

    Article  CAS  PubMed  Google Scholar 

  • Elliott J et al (2014) Constraints and potentials of future irrigation water availability on agricultural production under climate change. Proc Natl Acad Sci 111:3239–3244

    Article  CAS  PubMed  Google Scholar 

  • Evans JR (2013) Improving photosynthesis. Plant Physiol 162:1780–1793

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Evans JR, Loreto F (2000) Acquisition and diffusion of CO2 in higher plant leaves. In: Photosynthesis. Springer, Dordrecht, pp 321–351

    Chapter  Google Scholar 

  • Evans L, Rawson HM (1970) Photosynthesis and respiration by the flag leaf and components of the ear during grain development in wheat. Aust J Biol Sci 23:245–254

    Article  Google Scholar 

  • Fankhauser N, Aubry S (2016) Post-transcriptional regulation of photosynthetic genes is a key driver of C4 leaf ontogeny. J Exp Bot 68(2):137–146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fatichi S, Leuzinger S, Körner C (2014) Moving beyond photosynthesis: from carbon source to sink-driven vegetation modeling. New Phytol 201:1086–1095

    Article  CAS  PubMed  Google Scholar 

  • Feldman AB, Leung H, Baraoidan M, Elmido-Mabilangan A, Canicosa I, Quick WP, Sheehy J, Murchie EH (2017) Increasing leaf vein density via mutagenesis in rice results in an enhanced rate of photosynthesis, smaller cell sizes and can reduce interveinal mesophyll cell number. Front Plant Sci 8:1883

    Article  PubMed  PubMed Central  Google Scholar 

  • Foyer CH, Bloom AJ, Queval G, Noctor G (2009) Photorespiratory metabolism: genes, mutants, energetics, and redox signaling. Ann Rev Plant Biol 60:455–484

    Article  CAS  Google Scholar 

  • Furbank RT (2011) Evolution of the C4 photosynthetic mechanism: are there really three C4 acid decarboxylation types?. J Exp Bot 62(9):3103–3108

    Article  CAS  PubMed  Google Scholar 

  • Furbank RT (2016) Walking the C4 pathway: past, present, and future. J Exp Bot 67(14):4057–4066

    Article  CAS  PubMed  Google Scholar 

  • Furbank RT, Quick WP, Sirault XR (2015) Improving photosynthesis and yield potential in cereal crops by targeted genetic manipulation: prospects, progress and challenges. Field Crops Res 182:19–29

    Article  Google Scholar 

  • Galmes J, Kapralov MV, Andralojc P, Conesa MÀ, Keys AJ, Parry MA, Flexas J (2014) Expanding knowledge of the Rubisco kinetics variability in plant species: environmental and evolutionary trends Plant. Cell Environ 37:1989–2001

    Article  CAS  Google Scholar 

  • Gao X, Wang C, Cui H (2014) Identification of bundle sheath cell fate factors provides new tools for C3-to-C4 engineering. Plant Signal Behav 9:319–327

    Article  CAS  Google Scholar 

  • Gowik U, Westhoff P (2011) The path from C3 to C4 photosynthesis. Plant Physiology 155:56–63

    Article  CAS  PubMed  Google Scholar 

  • Gowik U, Schulze S, Saladié M, Rolland V, Tanz SK, Westhoff P, Ludwig M (2016) A MEM1-like motif directs mesophyll cell-specific expression of the gene encoding the C4 carbonic anhydrase in Flaveria. J Exp Bot 68(2):311–320

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Griffiths CA, Sagar R, Geng Y, Primavesi LF, Patel MK, Passarelli MK, Gilmore IS, Steven RT, Bunch J, Paul MJ, Davis BG (2016) Chemical intervention in plant sugar signalling increases yield and resilience. Nature 540(7634):574

    Article  CAS  PubMed  Google Scholar 

  • Gu L, Sun Y (2014) Artefactual responses of mesophyll conductance to CO2 and irradiance estimated with the variable J and online isotope discrimination methods Plant. Cell Environ 37:1231–1249

    Article  CAS  Google Scholar 

  • Hagemann M, Weber AP, Eisenhut M (2016) Photorespiration: origins and metabolic integration in interacting compartments. J Exp Bot 67:2915

    Article  CAS  PubMed Central  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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hatch M, Kagawa T, Craig S (1975) Subdivision of C4-pathway species based on differing C4 acid decarboxylating systems and ultrastructural features. Funct Plant Biol 2:111–128

    Article  CAS  Google Scholar 

  • Hattersley P (1984) Characterization of C4 type leaf anatomy in grasses (Poaceae). Mesophyll: bundle sheath area ratios. Ann Bot 53:163–180

    Article  Google Scholar 

  • Hibberd JM, Covshoff S (2010) The regulation of gene expression required for C4 photosynthesis. Annu Rev Plant Biol 61:181–207

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hoshida H, Tanaka Y, Hibino T, Hayashi Y, Tanaka A, Takabe T, Takabe T (2000) Enhanced tolerance to salt stress in transgenic rice that overexpresses chloroplast glutamine synthetase. Plant Mol Biol 43:103–111

    Article  CAS  PubMed  Google Scholar 

  • Hylton CM, Rawsthorne S, Smith AM, Jones DA, Woolhouse HW (1988) Glycine decarboxylase is confined to the bundle-sheath cells of leaves of C3–C4 intermediate species. Planta 175:452–459

    Article  CAS  PubMed  Google Scholar 

  • Imaizumi N, Usuda H, Nakamoto H, Ishihara K (1990) Changes in the rate of photosynthesis during grain filling and the enzymatic activities associated with the photosynthetic carbon metabolism in rice panicles. Plant Cell Physiol 31:835–844

    CAS  Google Scholar 

  • John CR, Smith-Unna RD, Woodfield H, Covshoff S, Hibberd JM (2014) Evolutionary convergence of cell-specific gene expression in independent lineages of C4 grasses. Plant Physiol 165:62–75

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kajala K et al (2011) Strategies for engineering a two-celled C4 photosynthetic pathway into rice. J Exp Bot 62:3001–3010

    Article  CAS  PubMed  Google Scholar 

  • Kanai R, Edwards G (1999) The biochemistry of C4 photosynthesis. In: Sage RF, Monson RK (eds) C4 plant biology. Academic Press, San Diego, pp 49–87

    Chapter  Google Scholar 

  • Kangasjärvi S, Neukermans J, Li S, Aro E-M, Noctor G (2012) Photosynthesis, photorespiration, and light signalling in defence responses. J Exp Bot 63:1619–1636

    Article  CAS  PubMed  Google Scholar 

  • Kausch AP, Owen TP, Zachwieja SJ, Flynn AR, Sheen J (2001) Mesophyll-specific, light and metabolic regulation of the C4 PPCZm1 promoter in transgenic maize. Plant Mol Biol 45:1–15

    Article  CAS  PubMed  Google Scholar 

  • Keys AJ (2006) The re-assimilation of ammonia produced by photorespiration and the nitrogen economy of C3 higher plants. Photosynth Res 87:165

    Article  CAS  PubMed  Google Scholar 

  • Kiang NY, Siefert J, Blankenship RE (2007) Spectral signatures of photosynthesis I. Review of Earth Organ Astrobiol 7:222–251

    Article  CAS  Google Scholar 

  • Kriedemann P (1966) The photosynthetic activity of the wheat ear. Ann Bot 30:349–363

    Article  CAS  Google Scholar 

  • Kromdijk J, Głowacka K, Leonelli L, Gabilly ST, Iwai M, Niyogi KK, Long SPJS (2016) Improving photosynthesis and crop productivity by accelerating recovery from photoprotection 354:857–861

    CAS  Google Scholar 

  • Kropff MJ, Cassman KG, Peng S, Matthews RB, Setter TL (1994) Quantitative understanding of yield potential. In: Cassman KG (ed) Breaking the yield barrier. IRRI, Los Banos, Philippines, pp 21–38

    Google Scholar 

  • Ku S, Gutierrez M, Kanai R, Edwards G (1974) Photosynthesis in mesophyll protoplasts and bundle sheath cells of various types of C4 plants II. Chlorophyll and hill reaction studies. Zeitschrift für Pflanzenphysiologie 72:320–337

    Article  CAS  Google Scholar 

  • Ku MS et al (2000) Photosynthetic performance of transgenic rice plants overexpressing maize C 4 photosynthesis enzymes. Stud Plant Sci 7:193–204

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Langdale JA, Nelson T (1991) Spatial regulation of photosynthetic development in C4 plants. Trends in Genetics 7:191–196

    Article  CAS  PubMed  Google Scholar 

  • Langdale JA, Lane B, Freeling M, Nelson T (1989) Cell lineage analysis of maize bundle sheath and mesophyll cells. Dev Biol 133(1):128–139

    Article  CAS  PubMed  Google Scholar 

  • Li J, Hu J (2015) Using co-expression analysis and stress-based screens to uncover Arabidopsis peroxisomal proteins involved in drought response. PloS One 10:e0137762

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li P et al (2010) The developmental dynamics of the maize leaf transcriptome. Nat Genet 42:1060–1067

    Article  CAS  PubMed  Google Scholar 

  • Li Y et al (2015) Developmental genetic mechanisms of C 4 syndrome based on transcriptome analysis of c 3 cotyledons and c 4 assimilating shoots in haloxylon ammodendron. PloS One 10:e0117175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Heckmann D, Lercher MJ, Maurino VG (2017) Combining genetic and evolutionary engineering to establish C4 metabolism in C3 plants. J Exp Bot 68:117–125

    Article  CAS  PubMed  Google Scholar 

  • Linka M, Weber AP (2005) Shuffling ammonia between mitochondria and plastids during photorespiration. Trends Plant Sci 10:461–465

    Article  CAS  PubMed  Google Scholar 

  • Long SP, Spence AK (2013) Toward cool C4 crops. Annu Rev Plant Biol 64:701–722

    Article  CAS  PubMed  Google Scholar 

  • Long SP, ZHU XG, Naidu SL, Ort DR (2006) Can improvement in photosynthesis increase crop yields? Plant Cell Environ 29:315–330

    Article  CAS  PubMed  Google Scholar 

  • Lovell JT et al (2016) Drought responsive gene expression regulatory divergence between upland and lowland ecotypes of a perennial C4 grass. Genome Res 26:510–518

    Article  CAS  PubMed  PubMed Central  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, van Wijk KJ (2009) Cell-type-specific differentiation of chloroplasts in C4 plants. Trends Plant Sci 14:100–109

    Article  CAS  PubMed  Google Scholar 

  • Majeran W et al (2010) Structural and metabolic transitions of C4 leaf development and differentiation defined by microscopy and quantitative proteomics in maize. Plant Cell 22(11):3509–3542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mallmann J, Heckmann D, Bräutigam A, Lercher MJ, Weber AP, Westhoff P, Gowik U (2014) The role of photorespiration during the evolution of C4 photosynthesis in the genus Flaveria. Elife 3:e02478

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matsuoka M, Furbank RT, Fukayama H, Miyao M (2001) Molecular engineering of C4 photosynthesis. Annu Rev Plant Biol 52:297–314

    Article  CAS  Google Scholar 

  • Maydup ML, Antonietta M, Guiamet J, Graciano C, López JR, Tambussi EA (2010) The contribution of ear photosynthesis to grain filling in bread wheat (Triticum aestivum L.). Field Crops Res 119:48–58

    Article  Google Scholar 

  • McKown AD, Dengler NG (2007) Key innovations in the evolution of Kranz anatomy and C4 vein pattern in Flaveria (Asteraceae). Am J Bot 94:382–399

    Article  PubMed  Google Scholar 

  • McKown AD, Dengler NG (2009) Shifts in leaf vein density through accelerated vein formation in C4 Flaveria (Asteraceae). Ann Bot 104:1085–1098

    Article  PubMed  PubMed Central  Google Scholar 

  • Merah O, Deleens E, Nachit M, Monneveux P (2001) Carbon isotope discrimination, leaf characteristics and grain yield of interspecific wheat lines and their durum parents under Mediterranean conditions. Cereal Res Commun 29:143–149

    Google Scholar 

  • Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci 11:15–19

    Article  CAS  PubMed  Google Scholar 

  • Monneveux P, Reynolds M, González-Santoyo H, Pena R, Mayr L, Zapata F (2004) Relationships between grain yield, flag leaf morphology, carbon isotope discrimination and ash content in irrigated wheat. J Agron Crop Sci 190:395–401

    Article  Google Scholar 

  • Muhaidat R, Sage RF, Dengler NG (2007) Diversity of Kranz anatomy and biochemistry in C4 eudicots. Am J Bot 94:362–381

    Article  CAS  PubMed  Google Scholar 

  • Muhaidat R, Sage TL, Frohlich MW, 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 34:1723–1736

    Article  CAS  PubMed  Google Scholar 

  • Naidu SL, Moose SP, Al-Shoaibi AK, Raines CA, Long SP (2003) Cold tolerance of C4 photosynthesis in Miscanthus × giganteus: adaptation in amounts and sequence of C4 photosynthetic enzymes. Plant Physiol 132:1688–1697

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nawarathna R, Dassanayake K, Nissanka S (2017) Is phenotypic variability in leaf vein density in rice associated with grain yield scientific. J Rice Res 1:1–9

    Google Scholar 

  • Niinemets Ü, Berry JA, Caemmerer S, Ort DR, Parry MA, Poorter H (2017) Photosynthesis: ancient, essential, complex, diverse… and in need of improvement in a changing world. New Phytol 213:43–47

    Article  PubMed  Google Scholar 

  • Noblin X, Mahadevan L, Coomaraswamy I, Weitz DA, Holbrook NM, Zwieniecki MA (2008) Optimal vein density in artificial and real leaves. Proc Natl Acad Sci 105:9140–9144

    Article  PubMed  Google Scholar 

  • Nutbeam AR, Duffus CM (1976) Evidence for C 4 photosynthesis in barley pericarp tissue. Biochem Biophys Res Commun 70:1198–1203

    Article  CAS  PubMed  Google Scholar 

  • Ort DR, Zhu X, Melis A (2011) Optimizing antenna size to maximize photosynthetic efficiency. Plant Physiol 155:79–85

    Article  CAS  PubMed  Google Scholar 

  • Ort DR et al (2015) Redesigning photosynthesis to sustainably meet global food and bioenergy demand 112:8529–8536

    CAS  Google Scholar 

  • Paterson AH et al (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457:551–556

    Article  CAS  PubMed  Google Scholar 

  • Pengelly JJ, Kwasny S, Bala S, Evans JR (2011) Functional analysis of corn husk photosynthesis. Plant physiol 156:503–513

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pick TR et al (2011) Systems analysis of a maize leaf developmental gradient redefines the current C4 model and provides candidates for regulation. Plant Cell 23:4208–4220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Piedade M, Junk W, Long S (1991) The productivity of the C_4 Grass Echinochloa polystachya on the Amazon floodplain. Ecology 72:1456–1463

    Article  Google Scholar 

  • Prendergast H, Hattersley P, Stone N (1987) New structural/biochemical associations in leaf blades of C4 grasses (Poaceae). Funct Plant Biol 14:403–420

    Article  CAS  Google Scholar 

  • Price GD, Badger MR, von Caemmerer S (2011) The prospect of using cyanobacterial bicarbonate transporters to improve leaf photosynthesis in C3 crop plants. Plant Physiol 155:20–26

    Article  CAS  PubMed  Google Scholar 

  • Rachmilevitch S, Cousins AB, Bloom AJ (2004) Nitrate assimilation in plant shoots depends on photorespiration. Proc Natl Acad Sci 101:11506–11510

    Article  CAS  PubMed  Google Scholar 

  • Rangan P, Furtado A, Henry RJ (2016a) Commentary: new evidence for grain specific C4 photosynthesis in wheat. Front Plant Sci 7:1537

    Article  PubMed  PubMed Central  Google Scholar 

  • Rangan P, Furtado A, Henry RJ (2016b) New evidence for grain specific C4 photosynthesis in wheat. Sci Rep 6:31721

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reeves G, Grangé-Guermente MJ, Hibberd JM (2016) Regulatory gateways for cell-specific gene expression in C4 leaves with Kranz anatomy. J Exp Bot 68(2):107–116

    Article  CAS  PubMed  Google Scholar 

  • Retkute R et al (2015) Exploiting heterogeneous environments: does photosynthetic acclimation optimize carbon gain in fluctuating light? J Exp Bot 66:2437–2447

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reyes-Prieto A, Weber AP, Bhattacharya D (2007) The origin and establishment of the plastid in algae and plants. Annu Rev Genet 41:147–168

    Article  CAS  PubMed  Google Scholar 

  • Rojas CM, Senthil-Kumar M, Wang K, Ryu C-M, Kaundal A, Mysore KS (2012) Glycolate oxidase modulates reactive oxygen species–mediated signal transduction during nonhost resistance in Nicotiana benthamiana and Arabidopsis. Plant Cell 24(1):336–352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rontein D, Rhodes D, Hanson AD (2003) Evidence from engineering that decarboxylation of free serine is the major source of ethanolamine moieties in plants. Plant Cell Physiol 44:1185–1191

    Article  CAS  PubMed  Google Scholar 

  • Roth-Nebelsick A, Uhl D, Mosbrugger V, Kerp H (2001) Evolution and function of leaf venation architecture: a review. Ann Bot 87:553–566

    Article  Google Scholar 

  • Sáez PL et al (2017) Photosynthetic limitations in two Antarctic vascular plants: importance of leaf anatomical traits and Rubisco kinetic parameters. J Exp Bot 68:2871–2883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sage RF (2002) C4 photosynthesis in terrestrial plants does not require Kranz anatomy. Trends Plant Sci 7:283–285

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Sage RF (2016) A portrait of the C4 photosynthetic family on the 50th anniversary of its discovery: species number, evolutionary lineages, and Hall of Fame. J Exp Bot 67:4039–4056

    Article  CAS  PubMed  Google Scholar 

  • Sage RF, Monson RK (1998) C4 plant biology. Elsevier

  • 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 50:756–772

    Article  CAS  PubMed  Google Scholar 

  • Sage RF, Christin P-A, Edwards EJ (2011) The C4 plant lineages of planet Earth. J Exp Bot 62:3155–3169

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Scarpella E, Marcos D, Friml J, Berleth T (2006) Control of leaf vascular patterning by polar auxin transport. Genes Devt 20:1015–1027

    Article  CAS  Google Scholar 

  • Schnable PS et al (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112–1115

    Article  CAS  PubMed  Google Scholar 

  • Schuler ML, Mantegazza O, Weber AP (2016) Engineering C4 photosynthesis into C3 chassis in the synthetic biology age. Plant J 87(1):51–65

    Article  CAS  PubMed  Google Scholar 

  • Sedelnikova OV, Hughes TE, Langdale JA (2018) Understanding the genetic basis of C4 Kranz anatomy with a view to engineering C3 crops. Annu Rev Genet 52:249–270

    Article  CAS  PubMed  Google Scholar 

  • Sharkey TD (1988) Estimating the rate of photorespiration in leaves. Physiol Plant 73:147–152

    Article  CAS  Google Scholar 

  • Sharwood RE, Ghannoum O, Kapralov MV, Gunn LH, Whitney SM (2016) Temperature responses of Rubisco from Paniceae grasses provide opportunities for improving C3 photosynthesis. Nat Plants 2:16186

    Article  CAS  PubMed  Google Scholar 

  • Sheehy JE, Ferrer AB, Mitchell P (2008) Harnessing photosynthesis in tomorrow’s world: Humans, crop production and poverty alleviation. In: Photosynthesis. Energy from the sun. Springer, Dordrecht, pp 1237–1242

    Chapter  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Sheen J-Y, Bogorad L (1987) Differential expression of C4 pathway genes in mesophyll and bundle sheath cells of greening maize leaves. J Biol Chem 262:11726–11730

    CAS  PubMed  Google Scholar 

  • Somerville CR (2001) An early Arabidopsis demonstration. Resolving a few issues concerning photorespiration. Plant Physiol 125:20–24

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Soros CL, Dengler NG (1998) Quantitative leaf anatomy of C3 and C4 Cyperaceae and comparisons with the Poaceae. Int J Plant Sci 159(3):480–491

    Article  Google Scholar 

  • South PF, Cavanagh AP, Liu HW, Ort DR (2019) Synthetic glycolate metabolism pathways stimulate crop growth and productivity in the field. Science 363:eaat9077

    Article  CAS  PubMed  Google Scholar 

  • Stapper M, Fischer R (1990) Genotype, sowing date and plant spacing influence on high-yielding irrigated wheat in southern New South Wales II. Growth, yield and nitrogen use. Aust J Agric Res 41:1021–1041

    Article  Google Scholar 

  • Stata M et al (2014) Mesophyll cells of C4 plants have fewer chloroplasts than those of closely related C3 plants. Plant Cell Environ 37:2587–2600

    Article  CAS  PubMed  Google Scholar 

  • Still CJ, Berry JA, Collatz GJ, DeFries RS (2003) Global distribution of C3 and C4 vegetation: carbon cycle implications. Glob Biogeochem Cycles 17(1):6–1

    Article  CAS  Google Scholar 

  • Sugiura D, Watanabe CK, Betsuyaku E, Terashima I (2017) Sink-Source Balance and Down-Regulation of Photosynthesis in Raphanus sativus: Effects of Grafting, N and CO2. Plant Cell Physiol 58:2043–2056

    Article  CAS  PubMed  Google Scholar 

  • Sunil M, Hariharan AK, Nayak S, Gupta S, Nambisan SR, Gupta RP, Panda B, Choudhary B, Srinivasan S (2014) The draft genome and transcriptome of Amaranthus hypochondriacus: a C4 dicot producing high-lysine edible pseudo-cereal. DNA Res 21(6):585–602

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taler D, Galperin M, Benjamin I, Cohen Y, Kenigsbuch D (2004) Plant eR genes that encode photorespiratory enzymes confer resistance against disease. Plant Cell 16:172–184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taniguchi M et al (2000) Binding of cell type-specific nuclear proteins to the 5′-flanking region of maize C4 phosphoenolpyruvate carboxylase gene confers its differential transcription in mesophyll cells. Plant Mol Biol 44:543–557

    Article  CAS  PubMed  Google Scholar 

  • Taylor SH, Long SP (2017) Slow induction of photosynthesis on shade to sun transitions in wheat may cost at least 21% of productivity. Phil Trans R Soc B 372:20160543

    Article  CAS  PubMed  Google Scholar 

  • Tcherkez G, Bligny R, Gout E, Mahé A, Hodges M, Cornic G (2008) Respiratory metabolism of illuminated leaves depends on CO2 and O2 conditions. Proc Nat Acad Sci 105:797–802

    Article  PubMed  Google Scholar 

  • Tholen D, Boom C, Noguchi K, Ueda S, Katase T, Terashima I (2008) The chloroplast avoidance response decreases internal conductance to CO2 diffusion in Arabidopsis thaliana leaves. Plant Cell Environ 31:1688–1700

    Article  CAS  PubMed  Google Scholar 

  • Tilman D et al (2009) Beneficial biofuels—the food, energy, and environment trilemma. Science 325:270–271

    Article  CAS  PubMed  Google Scholar 

  • Tosens T et al (2016) The photosynthetic capacity in 35 ferns and fern allies: mesophyll CO2 diffusion as a key trait. New Phytol 209:1576–1590

    Article  CAS  PubMed  Google Scholar 

  • Ueno O (1998) Induction of Kranz anatomy and C4-like biochemical characteristics in a submerged amphibious plant by abscisic acid. Plant Cell 10:571–583

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ueno O, Yoshimura Y, Sentoku N (2005) Variation in the activity of some enzymes of photorespiratory metabolism in C4 grasses. Ann Bot 96:863–869

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vialet-Chabrand S, Matthews JS, Simkin AJ, Raines CA, Lawson T (2017) Importance of fluctuations in light on plant photosynthetic acclimation. Plant Physiol 173:2163–2179

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • von Caemmerer S (2003) C4 photosynthesis in a single C3 cell is theoretically inefficient but may ameliorate internal CO2 diffusion limitations of C3 leaves Plant. Cell Environt 26:1191–1197

    Article  Google Scholar 

  • von Caemmerer S, Evans JR (2010) Enhancing C 3 photosynthesis. Plant Physiol 154:589–592

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • von Caemmerer S, Quick WP, Furbank RT (2012) The development of C4 rice: current progress and future challenges. Science 336:1671–1672

    Article  CAS  Google Scholar 

  • S Von Caemmerer, Ghannoum O, Pengelly JJ, Cousins AB (2014) Carbon isotope discrimination as a tool to explore C4 photosynthesis. J Exp Bot 65:3459–3470

    Article  Google Scholar 

  • von Caemmerer S, Ghannoum O, Furbank RT (2017) C4 photosynthesis: 50 years of discovery and innovation. J Exp Bot 68:97–102

    Article  CAS  Google Scholar 

  • Voss I, Sunil B, Scheibe R, Raghavendra A (2013) Emerging concept for the role of photorespiration as an important part of abiotic stress response. Plant Biol 15:713–722

    Article  CAS  PubMed  Google Scholar 

  • Voznesenskaya EV, Franceschi VR, Kiirats O, Freitag H, Edwards GE (2001a) Kranz anatomy is not essential for terrestrial C4 plant photosynthesis. Nature 414:543–546

    Article  CAS  PubMed  Google Scholar 

  • Voznesenskaya EV, Franceschi VR, Kiirats O, Freitag H, Edwards GE (2001b) Kranz anatomy is not essential for terrestrial C 4 plant photosynthesis. Nature 414:543

    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 31:649–662

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Peterson RB, Brutnell TP (2011) Regulatory mechanisms underlying C4 photosynthesis. New Phytol 190:9–20

    Article  CAS  PubMed  Google Scholar 

  • Wang P, Kelly S, Fouracre JP, Langdale JA (2013) Genome-wide transcript analysis of early maize leaf development reveals gene cohorts associated with the differentiation of C4 K Ranz anatomy. Plant J 75(4):656–670

    Article  CAS  PubMed  Google Scholar 

  • Wang L et al (2014) Comparative analyses of C4 and C3 photosynthesis in developing leaves of maize and rice. Nat Biotechnol 32:1158–1165

    Article  CAS  PubMed  Google Scholar 

  • Wang P, Khoshravesh R, Karki S, Tapia R, Balahadia CP, Bandyopadhyay A, Quick WP, Furbank R, Sage TL, Langdale JA (2017a) Recreation of a key step in the evolutionary switch from C3 to C4 leaf anatomy. Curr Biol 27(21):3278–3287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang S, Tholen D, Zhu XG (2017b) C4 photosynthesis in C3 rice: a theoretical analysis of biochemical and anatomical factors Plant. Cell Environ 40:80–94

    Article  CAS  Google Scholar 

  • Weber AP, von Caemmerer S (2010) Plastid transport and metabolism of C 3 and C 4 plants—comparative analysis and possible biotechnological exploitation. Curr Opin Plant Biol 13:256–264

    Article  CAS  Google Scholar 

  • Williams M, Rastetter EB, Van der Pol L, Shaver GR (2014) Arctic canopy photosynthetic efficiency enhanced under diffuse light, linked to a reduction in the fraction of the canopy in deep shade. New Phytol 202:1267–1276

    Article  CAS  PubMed  Google Scholar 

  • Wong S-C, Cowan IR, Farquhar GD (1985) Leaf conductance in relation to rate of CO2 assimilation I. Influence of nitrogen nutrition, phosphorus nutrition, photon flux density, and ambient partial pressure of CO2 during ontogeny. Plant Physiol 78:821–825

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Worldmeters (2017) Worldmeters. http://www.worldometers.info/. Accessed 02 Feb 2017

  • Xiong D, Flexas J, Yu T, Peng S, Huang J (2017) Leaf anatomy mediates coordination of leaf hydraulic conductance and mesophyll conductance to CO2 in Oryza. New Phytol 213:572–583

    Article  CAS  PubMed  Google Scholar 

  • Yakir D, Osmond B, Giles L (1991) Autotrophy in maize husk leaves: evaluation using natural abundance of stable isotopes. Plant physiol 97:1196–1198

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamori W, Hikosaka K, Way DA (2014) Temperature response of photosynthesis in C3, C4, and CAM plants: temperature acclimation and temperature adaptation. Photosynth Res 119:101–117

    Article  CAS  PubMed  Google Scholar 

  • Yoshimura Y, Kubota F, Ueno O (2004) Structural and biochemical bases of photorespiration in C4 plants: quantification of organelles and glycine decarboxylase. Planta 220:307–317

    Article  CAS  PubMed  Google Scholar 

  • Yuan D (2012) Biotechnological interventions for crop improvement in the context of food security. Doctoral dissertation, Universitat de Lleida

  • Zachos JC, Dickens GR, Zeebe RE (2008) An early Cenozoic perspective on greenhouse warming and carbon-cycle dynamics. Nature 451:279–283

    Article  CAS  PubMed  Google Scholar 

  • Zhang G et al (2012a) Genome sequence of foxtail millet (Setaria italica) provides insights into grass evolution and biofuel potential. Nat Biotechnol 30:549–554

    Article  CAS  PubMed  Google Scholar 

  • Zhang S-B, Guan Z-J, Sun M, Zhang J-J, Cao K-F, Hu H (2012b) Evolutionary association of stomatal traits with leaf vein density in Paphiopedilum, Orchidaceae. PloS One 7:e40080

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu XG, Portis A Jr, Long S (2004) Would transformation of C3 crop plants with foreign Rubisco increase productivity? A computational analysis extrapolating from kinetic properties to canopy photosynthesis. Plant Cell Environ 27:155–165

    Article  CAS  Google Scholar 

  • Zhu X-G, Long SP, Ort DR (2008) What is the maximum efficiency with which photosynthesis can convert solar energy into biomass? Curr Opin Biotechnol 19:153–159

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the University of Southern Queensland (USQ), Australia, and the USQ Strategic Research Fund. PD is supported by a USQ International Stipend Research Scholarship and USQ International Fees Research Scholarship.

Author information

Authors and Affiliations

  1. Centre for Crop Health, University of Southern Queensland, Toowoomba, QLD, 4350, Australia

    Prabuddha Dehigaspitiya, Gavin J. Ash, Kiruba Arun-Chinnappa, Dananjali Gamage, Anke Martin, Seiji Nagasaka & Saman Seneweera

  2. Hawkesbury Institute for the Environment, Western Sydney University, LB 1797, Penrith, NSW, 2753, Australia

    Paul Milham

  3. National Institute of Fundamental Studies, Hanthana Road, Kandy, 20000, Central, Sri Lanka

    Saman Seneweera

Authors
  1. Prabuddha Dehigaspitiya
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Paul Milham
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gavin J. Ash
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kiruba Arun-Chinnappa
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Dananjali Gamage
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Anke Martin
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Seiji Nagasaka
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Saman Seneweera
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Saman Seneweera.

Ethics declarations

Conflict of interest

The authors declare that this study was conducted in the absence of any commercial relationships that could lead to any potential conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dehigaspitiya, P., Milham, P., Ash, G.J. et al. Exploring natural variation of photosynthesis in a site-specific manner: evolution, progress, and prospects. Planta 250, 1033–1050 (2019). https://doi.org/10.1007/s00425-019-03223-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-019-03223-1

Keywords

Search

Navigation