Skip to main content

Advertisement

Log in

Genetic analysis and phenotypic characterization of leaf photosynthetic capacity in a sorghum (Sorghum spp.) diversity panel

  • Research Article
  • Published:
Genetic Resources and Crop Evolution Aims and scope Submit manuscript

Abstract

Carbon assimilation is the fundamental basis of crop productivity, but this important and complex trait has not been genetically characterized and directly exploited at the commercial level to improve yield. Therefore, there is a critical need to determine natural genetic variation in carbon assimilation, to advance our knowledge of the genetic mechanisms controlling this trait and, on that basis, to develop germplasm with superior photosynthetic capacity. Sorghum is the most productive annual species for biofuel production in which leaf photosynthetic capacity has been associated with biomass yield. In this study, a set of 82 sorghum accessions was genetically characterized and phenotypically evaluated for carbon assimilation (A), stomatal conductance (gs), transpiration rate (T), efficiency of energy capture by open PSII reaction centers (Fv′/Fm′), effective quantum yield (ΦPSII) and photochemical quenching (qP). Phenotypic variation was observed for all traits, with A ranging from 11.6 to 42.5 µmol CO2 m−2 s−1. The highest positive correlations were between A and ΦPSII (r = 0.71), gs and T (r = 0.89) and ΦPSII and qP (r = 0.91). The highest negative correlations were between gs and A/gs (r = −0.82), T and A/gs (r = −0.79), T and A/T (r = −0.79) and A/gs and A/T (r = −0.78). Population structure and cluster analysis clearly differentiated three subpopulations among this set of accessions with significantly different values for A, gs and Fv′/Fm′. This study demonstrates that this diverse set of sorghum accessions could be utilized to identify genes/markers associated with variation in leaf photosynthetic rate and could be exploited in breeding programs to develop germplasm with superior carbon assimilation capacity.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

A :

Leaf photosynthetic rate (µmol CO2 m−2 s−1)

gs :

Stomatal conductance (mol H2O m−2 s−1)

T:

Transpiration rate (mmol H2O m−2 s−1)

Fv′/Fm′:

Efficiency of energy capture by open PSII reaction centers (unitless)

ΦPSII :

Effective quantum yield (unitless)

qP:

Photochemical quenching (unitless)

A/gs :

Intrinsic leaf water use efficiency (µmol mol−1)

A/T:

Transpiration ratio (µmol mmol−1)

PAR:

Photosynthetically active radiation

References

  • Agrama HA, Eizenga GC, Yan W (2007) Association mapping of yield and its components in rice cultivars. Mol Breed 19:341–356

    Article  Google Scholar 

  • Andersen JR, Schrag T, Melchinger AE, Zein I, Lubberstedt T (2005) Validation of Dwarf8 polymorphisms associated with flowering time in elite European inbred lines of maize (Zea mays L.). Theor Appl Genet 111:206–217

    Article  CAS  PubMed  Google Scholar 

  • Aranzana MJ, Kim S, Zhao K, Bakker E, Horton M, Jakob K, Lister C, Molitor J, Shindo C, Tang C, Toomajian C, Traw B, Zheng H, Bergelson J, Dean C, Marjoram P, Nordborg M (2005) Genome-wide association mapping in Arabidopsis identifies previously known flowering time and pathogen resistance genes. PLoS Genet 1:e60

    Article  PubMed Central  PubMed  Google Scholar 

  • Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113

    Article  CAS  PubMed  Google Scholar 

  • Balota M, Payne WA, Rooney W, Rosenow D (2008) Gas exchange and transpiration ratio in sorghum. Crop Sci 48:2361–2371

    Article  CAS  Google Scholar 

  • Bandyopadhyay A, Datta K, Zhang J, Yang W, Raychaudhuri S, Miyao M, Datta SK (2007) Enhanced photosynthesis rate in genetically engineered indica rice expressing pepc gene cloned from maize. Plant Sci 172:1204–1209

    Article  CAS  Google Scholar 

  • Botstein D, White RL, Skolnick M, Davis RW (1980) Construction of a genetic linkage map in man using restriction fragment length polymorphisms. Am J Hum Genet 32:314–331

    CAS  PubMed Central  PubMed  Google Scholar 

  • Breseghello F, Sorrells ME (2006) Association mapping of kernel size and milling quality in wheat (Triticum aestivum L.) cultivars. Genetics 172:1165–1177

    Article  PubMed Central  PubMed  Google Scholar 

  • Casa AM, Pressoir G, Brown PJ, Mitchell SE, Rooney WL, Tuinstra MR, Franks CD, Kresovich S (2008) Community resources and strategies for association mapping in sorghum. Crop Sci 48:30–40

    Article  Google Scholar 

  • Christman MA, Richards JH, McKay JK, Stahl EA, Juenger TE, Donovan LA (2008) Genetic variation in Arabidopsis thaliana for night-time leaf conductance. Plant Cell Environ 31:1170–1178

    Article  CAS  PubMed  Google Scholar 

  • Cousins AB, Adam NR, Wall GW, Kimball BA, Pinter PJ, Ottman MJ, Leavitt SW, Webber AN (2002) Photosystem II energy use, non-photochemical quenching and the xanthophyll cycle in Sorghum bicolor grown under drought and free-air CO2 enrichment (FACE) conditions. Plant Cell Environ 25:1551–1559

    Article  CAS  Google Scholar 

  • Crosbie TM, Pearce RB (1982) Effects of recurrent phenotypic selection for high and low photosynthesis on agronomic traits in two maize populations. Crop Sci 22:809–813

    Article  Google Scholar 

  • Dohleman FG, Long SP (2009) More productive than maize in the Midwest: how does Miscanthus do it? Plant Physiol 150:2104–2115

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15

    Google Scholar 

  • Ehrenreich IM, Stafford PA, Purugganan MD (2007) The genetic architecture of shoot branching in Arabidopsis thaliana: a comparative assessment of candidate gene associations vs. quantitative trait locus mapping. Genetics 176:1223–1236

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure: extensions to linked loci and correlated allele frequencies. Genetics 164:1567–1587

    CAS  PubMed Central  PubMed  Google Scholar 

  • Feng L, Wang K, Li Y, Tan Y, Kong J, Li H, Li Y, Zhu Y (2007) Overexpression of SBPase enhances photosynthesis against high temperature stress in transgenic rice plants. Plant Cell Rep 26:1635–1646

    Article  CAS  PubMed  Google Scholar 

  • Flint-Garcia SA, Thornsberry JM, Buckler ES (2003) Structure of linkage disequilibrium in plants. Annu Rev Plant Biol 54:357–374

    Article  CAS  PubMed  Google Scholar 

  • Flood PJ, Harbinson J, Aarts MGM (2011) Natural genetic variation in plant photosynthesis. Trends Plant Sci 16:327–335

    Article  CAS  PubMed  Google Scholar 

  • Fracheboud Y, Ribaut J, Vargas M, Messmer R, Stamp P (2002) Identification of quantitative trait loci for cold-tolerance of photosynthesis in maize (Zea mays L.). J Exp Bot 53:1967–1977

    Article  CAS  PubMed  Google Scholar 

  • Gilbert ME, Zwieniecki MA, Holbrook NM (2011) Independent variation in photosynthetic capacity and stomatal conductance leads to differences in intrinsic water use efficiency in eleven soybean genotypes before and during mild drought. J Exp Bot 62:2875–2887

    Article  CAS  PubMed  Google Scholar 

  • Guo P, Baum M, Varchney R, Graner A, Grando S, Ceccarelli S (2008) QTLs for chlorophyll and chlorophyll fluorescence parameters in barley under post-flowering drought. Euphytica 163:203–214

    Article  CAS  Google Scholar 

  • Hallam AL, Anderson C, Buxton DR (2001) Comparative economic analysis of perennial, annual and intercrops for biomass production. Biomass Bioenerg 21:407–424

    Article  Google Scholar 

  • Harrison EP, Willingham NM, Lloyd JC, Raines CA (1998) Reduced sedoheptulose-1,7-bisphosphatase levels in transgenic tobacco lead to decreased photosynthetic capacity and altered carbohydrate accumulation. Planta 204:27–36

    Article  CAS  Google Scholar 

  • Henderson S, von Caemmerer S, Farquhar GD, Wade L, Hammer G (1998) Correlation between carbon isotope discrimination and transpiration efficiency in lines of the C4 species Sorghum bicolor in the glasshouse and the field. Aust J Plant Physiol 25:111–123

    Article  Google Scholar 

  • Herve D, Berrios EF, Leroux N, Chaarani GA, PLanchon C, Sarrafi A, Gentzbittel L (2001) QTL analysis of photosynthesis and water status traits in sunflower (Helianthus annuus L.) under greenhouse conditions. J Exp Bot 52:1857–1864

    Article  CAS  PubMed  Google Scholar 

  • Hubbart S, Peng S, Horton P, Chen Y, Murchie EH (2007) Trends in leaf photosynthesis in historical rice varieties developed in the Philippines since 1966. J Exp Bot 58:3429–3438

    Article  CAS  PubMed  Google Scholar 

  • Kajala K, Covshoff S, Karki S, Woodfield H, Tolley BJ, Dionora MJ, Mogul RT, Mabilangan AE, Danila FR, Hibberd JM, Quick WP (2011) Strategies for engineering a two-celled C4 photosynthetic pathway into rice. J Exp Bot 62:3001–3010

    Article  CAS  PubMed  Google Scholar 

  • Kanemura T, Homma K, Ohsumi A, Shiraiwa T, Horie T (2007) Evaluation of genotypic variation in leaf photosynthetic rate and its associated factors by using a rice diversity research set of germplasm. Photosynth Res 94:23–30

    Article  CAS  PubMed  Google Scholar 

  • Kiani SP, Maury P, Sarrafi A, Grieu P (2008) QTL analysis of chlorophyll fluorescence parameters in sunflower (Helianthus annuus L.) under well-watered and water-stressed conditions. Plant Sci 175:565–573

    Article  Google Scholar 

  • Kidambi SP, Krieg DR, Rosenow DT (1990) Genetic variation for gas exchange rates in grain sorghum. Plant Physiol 92:1211–1214

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lefebvre S, Lawson T, Zakhleniuk OV, Lloyd JC, Raines CA (2005) Increased sedoheptulose-1,7-bisphosphatase activity in transgenic tobacco plants stimulates photosynthesis and growth from an early stage in development. Plant Physiol 138:451–460

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Liu K, Muse SV (2005) PowerMarker: integrated analysis environment for genetic marker data. Bioinformatics 21:2128–2129

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence a practical guide. J Exp Bot 51:659–668

    Article  CAS  PubMed  Google Scholar 

  • Miyao M, Masumoto C, Miyazawa S, Fukayama H (2011) Lessons from engineering a single-cell C4 photosynthetic pathway into rice. J Exp Bot 62:3021–3029

    Article  CAS  PubMed  Google Scholar 

  • Morris GP, Ramu P, Deshpande SP, Hash CT, Shah T, Upadhyaya HD, Riera-Lizarazu O, Brown PJ, Acharya CB, Mitchell SE, Harriman J, Glaubitz JC, Buckler ES, Kresovich S (2013) Population genomic and genome-wide association studies of agroclimatic traits in sorghum. Proc Natl Acad Sci USA 110:453–458

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Murray SC, Rooney WL, Hamblin MT, Mitchell SE, Kresovich S (2009) Sweet sorghum genetic diversity and association mapping for brix and height. Plant Genome 2:48–62

    Article  CAS  Google Scholar 

  • Myles S, Peiffer J, Brown PJ, Ersoz ES, Zhang Z, Costich DE, Buckler ES (2009) Association mapping: critical considerations shift from genotyping to experimental design. Plant Cell 2:2194–2202

    Article  Google Scholar 

  • Nei M, Takezaki N (1983) Estimation of genetic distances and phylogenetic trees from DNA analysis. In: Proceedings of the 5th World Congress on Genetics Applied to Livestock Production, vol 21, pp 405–412

  • Olsen KM, Halldorsdottir SS, Stinchcombe JR, Weinig C, Schmitt J, Purugganan MD (2004) Linkage disequilibrium mapping of Arabidopsis CRY2 flowering time alleles. Genetics 167:1361–1369

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Palaisa K, Morgante M, Tingey S, Rafalski A (2004) Long-range patterns of diversity and linkage disequilibrium surrounding the maize Y1 gene are indicative of an asymmetric selective sweep. Proc Natl Acad Sci USA 101:9885–9890

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Peng S, Krieg D (1992) Gas exchange and their relationship to water use efficiency of grain sorghum. Crop Sci 32:386–391

    Article  Google Scholar 

  • Peng S, Krieg DR, Girma FS (1991) Leaf photosynthetic rate is correlated with biomass and grain production in grain sorghum lines. Photosynth Res 28:1–7

    Article  CAS  PubMed  Google Scholar 

  • Pettigrew WT (2004) Cotton genotypic variation in the photosynthetic response to irradiance. Photosynthetica 42:567–571

    Article  CAS  Google Scholar 

  • Pettigrew WT, Gerik TJ (2007) Cotton leaf photosynthesis and carbon metabolism. Adv Agron 94:209–236

    Article  CAS  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rooney WL (2004) Sorghum improvement—integrating traditional and new technology to produce improved genotypes. Adv Agron 83:37–109

    Article  Google Scholar 

  • Rooney WL, Blumenthal J, Bean B, Mullet JE (2007) Designing sorghum as a dedicated bioenergy feedstock. Biofuel Bioprod Bior 1:147–157

    Article  CAS  Google Scholar 

  • Sadras VO, Lawson C, Montoro A (2012) Photosynthetic traits in Australian wheat varieties released between 1958 and 2007. Field Crop Res 134:19–29

    Article  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic tree. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Salas Fernandez MG (2008) Genetic and phenotypic characterization of carotenoid content in sorghum grain. PhD Dissertation, Cornell University. Ithaca, New York, USA

  • Salas Fernandez MG, Becraft PW, Yin Y, Lubberstedt T (2009a) From dwarves to giants? Plant height manipulation for biomass yield. Trends Plant Sci 14:454–461

    Article  CAS  PubMed  Google Scholar 

  • Salas Fernandez MG, Kapran I, Souley S, Abdou M, Maiga IH, Acharya CB, Hamblin MT, Kresovich S (2009b) Collection and characterization of yellow endosperm sorghums from West Africa for biofortification. Genet Resour Crop Evol 56:991–1000

    Article  Google Scholar 

  • Salvi S (2007) Conserved non-coding genomic sequences associated with a flowering-time quantitative trait locus in maize. Proc Natl Acad Sci USA 104:11376–11381

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Skot L, Humphreys MO, Armstead I, Heywood S, Skot KP, Sanderson R, Thomas ID, Chorlton KH, Hamilton NRS (2005) An association mapping approach to identify flowering time genes in natural populations of Lolium perenne L. Mol Breed 15:233–245

    Article  CAS  Google Scholar 

  • Sukumaran S, Xiang W, Bean SR, Pedersen JF, Kresovich S, Tuinstra MR, Tesso TT, Hamblin MT, Yu J (2012) Association mapping for grain quality in a diverse sorghum collection. Plant Genome 5:126–135

    Article  CAS  Google Scholar 

  • Suzuki S, Murai N, Burnell JN, Arai M (2000) Changes in photosynthetic carbon flow in transgenic rice plants that express C4-type phosphoenolpyruvate carboxykinase from Urochloa panicoides. Plant Physiol 124:163–172

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Szalma SJ, Buckler ES, Snook ME, McMullen MD (2005) Association analysis of candidate genes for maysin and chlorogenic acid accumulation in maize silks. Theor Appl Genet 110:1324–1333

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tanaka Y, Sugano SS, Shimada T, Hara-Nishimura I (2013) Enhancement of leaf photosynthetic capacity through increased stomatal density in Arabidopsis. New Phytol 198:757–764

    Article  CAS  PubMed  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

    Article  CAS  PubMed  Google Scholar 

  • Teng S, Qian Q, Zeng D, Kunihiro Y, Fujimoto K, Huang D, Zhu L (2004) QTL analysis of leaf photosynthetic rate and related physiological traits in rice (Oryza sativa L.). Euphytica 135:1–7

    Article  CAS  Google Scholar 

  • Thornsberry JM, Goodman MM, Doebley J, Kresovich S, Nielsen D, Buckler ES (2001) Dwarf8 polymorphisms associate with variation in flowering time. Nat Genet 28:286–289

    Article  CAS  PubMed  Google Scholar 

  • Tracy WF, Whitt SR, Buckler ES (2006) Recurrent mutation and genome evolution: example of Sugary 1 and the origin of sweet maize. Crop Sci 46:S49–S54

    Article  Google Scholar 

  • Yang D, Jing R, Chang X, Li W (2007) Quantitative loci mapping for chlorophyll fluorescence and associated traits in wheat (Triticum aestivum). J Integr Plant Biol 49:646–654

    Article  CAS  Google Scholar 

  • Yin Z, Meng F, Song H, Xu X, Yu D (2010) Mapping quantitative trait loci associated with chlorophyll a fluorescence. Planta 231:875–885

    Article  CAS  PubMed  Google Scholar 

  • Yu J, Buckler ES (2006) Genetic association mapping and genome organization of maize. Curr Opin Plant Biol 17:155–160

    CAS  Google Scholar 

  • Yu J, Pressoir G, Briggs WH, Bi IV, Yamasaki M, Doebley JF, McMullen MD, Gaut BS, Nielsen DM, Holland JB, Kresovich S, Buckler E (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38:203–208

    Article  CAS  PubMed  Google Scholar 

  • Zeng B, Xu X, Zhou S, Zhu C, Tang C (2012) Effects of temperature and light on photosynthetic heterosis of an upland cotton hybrid cultivar. Crop Sci 52:282–291

    Article  CAS  Google Scholar 

  • Zhu C, Gore M, Buckler ES, Yu J (2008) Status and prospects of association mapping in plants. Plant Genome 1:5–20

    Article  CAS  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

Acknowledgments

We would like to express our gratitude to Frank Dohleman and Whitney Bouma for their support and training in the use of Licor technology. This work was supported by the United States Department of Agriculture, National Institute of Food and Agriculture [Project#IOW05298] and the sorghum Checkoff Program [Contract No: R0007-11].

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Maria G. Salas Fernandez.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 114 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Salas Fernandez, M.G., Strand, K., Hamblin, M.T. et al. Genetic analysis and phenotypic characterization of leaf photosynthetic capacity in a sorghum (Sorghum spp.) diversity panel. Genet Resour Crop Evol 62, 939–950 (2015). https://doi.org/10.1007/s10722-014-0202-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10722-014-0202-6

Keywords

Navigation