Site-specific, genotypic and temporal variation in photosynthesis and its related biochemistry in wheat (Triticum aestivum)
Prabuddha Dehigaspitiya
A , Paul Milham B , Anke Martin A , Gavin Ash A , Dananjali Gamage C , Paul Holford D and Saman Seneweera A E *
+ Author Affiliations
- Author Affiliations
A Centre for Crop Health, University of Southern Queensland, Toowoomba, Qld 4350, Australia.
B Hawkesbury Institute for the Environment, Western Sydney University, LB 1797, Penrith, NSW 2753, Australia.
C Department of Agricultural Biology, Faculty of Agriculture, University of Ruhuna, Matara, Sri Lanka.
D School of Science, Western Sydney University, LB 1797, Penrith, NSW 2753, Australia.
E Faculty of Veterinary and Agriculture Science, University of Melbourne, Parkville, Vic. 3010, Australia.
Functional Plant Biology 49(2) 115-131 https://doi.org/10.1071/FP21111
Submitted: 13 April 2021 Accepted: 18 October 2021 Published: 14 December 2021
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)
Abstract
Photosynthesis in wheat (Triticum aestivum L.) pericarps may contribute appreciably to wheat grain yield. Consequently, we investigated the temporal variation of traits related to photosynthesis and sucrose metabolism in the pericarps and flag leaves of three wheat genotypes, Huandoy, Amurskaja 75 and Greece 25, which are reported to differ in expression of genes related to the C4 pathway in wheat grain. Significant site-specific, genotypic and temporal variation in the maximum carboxylation rate (Vcmax) and maximum rates of electron transport (Jmax) (biological capacity of carbon assimilation) were observed early in ontogeny that dissipated by late grain filling. Although the transcript abundance of rbcS and rbcL in flag leaves was significantly higher than in the pericarps, in line with their photosynthetic prominence, both organ types displayed similar expression patterns among growth stages. The higher N concentrations in the pericarps during grain enlargement suggest increased Rubisco; however, expression of rbcS and rbcL indicated the contrary. From heading to 14 days post-anthesis, wheat pericarps exhibited a strong, positive correlation between biological capacity for carbon assimilation and expression of key genes related to sucrose metabolism (SPS1, SUS1 and SPP1). The strong correlation between spike dry weight and the biological capacity for carbon assimilation along with other findings of this study suggest that metabolic processes in wheat spikes may play a major role in grain filling, total yield and quality.
Keywords: biological capacity of carbon assimilation, grain filling, Jmax, source and sink interaction, spike gas exchange, sucrose metabolism, transcript abundance, Vcmax.
References
Bachir DG, Saeed I, Song Q, Linn TZ, Chen L, Hu Y-G (2017) Characterization and expression patterns of key C4 photosynthetic pathway genes in bread wheat (Triticum aestivum L.) under field conditions. Journal of Plant Physiology 213, 87–97.| Characterization and expression patterns of key C4 photosynthetic pathway genes in bread wheat (Triticum aestivum L.) under field conditions.Crossref | GoogleScholarGoogle Scholar | 28340469PubMed |
Barbottin A, Lecomte C, Bouchard C, Jeuffroy M-H (2005) Nitrogen remobilization during grain filling in wheat: genotypic and environmental effects. Crop Science 45, 1141–1150.
| Nitrogen remobilization during grain filling in wheat: genotypic and environmental effects.Crossref | GoogleScholarGoogle Scholar |
Bate NJ, Rothstein SJ, Thompson JE (1991) Expression of nuclear and chloroplast photosynthesis-specific genes during leaf senescence. Journal of Experimental Botany 42, 801–811.
| Expression of nuclear and chloroplast photosynthesis-specific genes during leaf senescence.Crossref | GoogleScholarGoogle Scholar |
Battistelli A, Adcock MD, Leegood RC (1991) The relationship between the activation state of sucrose-phosphate synthase and the rate of CO2 assimilation in spinach leaves. Planta 183, 620–622.
| The relationship between the activation state of sucrose-phosphate synthase and the rate of CO2 assimilation in spinach leaves.Crossref | GoogleScholarGoogle Scholar | 24193857PubMed |
Baxter CJ, Foyer CH, Turner J, Rolfe SA, Quick WP (2003) Elevated sucrose-phosphate synthase activity in transgenic tobacco sustains photosynthesis in older leaves and alters development. Journal of Experimental Botany 54, 1813–1820.
| Elevated sucrose-phosphate synthase activity in transgenic tobacco sustains photosynthesis in older leaves and alters development.Crossref | GoogleScholarGoogle Scholar | 12815030PubMed |
Bihmidine S, Hunter CT, Johns CE, Koch KE, Braun DM (2013) Regulation of assimilate import into sink organs: update on molecular drivers of sink strength. Frontiers in Plant Science 4, 177
| Regulation of assimilate import into sink organs: update on molecular drivers of sink strength.Crossref | GoogleScholarGoogle Scholar | 23761804PubMed |
Coleman HD, Ellis DD, Gilbert M, Mansfield SD (2006) Up-regulation of sucrose synthase and UDP-glucose pyrophosphorylase impacts plant growth and metabolism. Plant Biotechnology Journal 4, 87–101.
| Up-regulation of sucrose synthase and UDP-glucose pyrophosphorylase impacts plant growth and metabolism.Crossref | GoogleScholarGoogle Scholar | 17177788PubMed |
Coleman HD, Yan J, Mansfield SD (2009) Sucrose synthase affects carbon partitioning to increase cellulose production and altered cell wall ultrastructure. Proceedings of the National Academy of Sciences 106, 13118–13123.
| Sucrose synthase affects carbon partitioning to increase cellulose production and altered cell wall ultrastructure.Crossref | GoogleScholarGoogle Scholar |
Craig J, Barratt P, Tatge H, Déjardin A, Handley L, Gardner CD, Barber L, Wang T, Hedley C, Martin C ((1999)) Mutations at the rug4 locus alter the carbon and nitrogen metabolism of pea plants through an effect on sucrose synthase. The Plant Journal 17, 353–362.
| Mutations at the rug4 locus alter the carbon and nitrogen metabolism of pea plants through an effect on sucrose synthase.Crossref | GoogleScholarGoogle Scholar |
Darroch BA, Baker RJ (1990) Grain filling in three spring wheat genotypes: statistical analysis. Crop Science 30, 525–529.
| Grain filling in three spring wheat genotypes: statistical analysis.Crossref | GoogleScholarGoogle Scholar |
Dean C, Pichersky E, Dunsmuir P (1989) Structure, evolution, and regulation of RbcS genes in higher plants. Annual Review of Plant Physiology and Plant Molecular Biology 40, 415–439.
| Structure, evolution, and regulation of RbcS genes in higher plants.Crossref | GoogleScholarGoogle Scholar |
Dehigaspitiya P, Milham P, Ash GJ, Arun-Chinnappa K, Gamage D, Martin A, Nagasaka S, Seneweera S (2019) Exploring natural variation of photosynthesis in a site-specific manner: evolution, progress, and prospects. Planta 250, 1033–1050.
| Exploring natural variation of photosynthesis in a site-specific manner: evolution, progress, and prospects.Crossref | GoogleScholarGoogle Scholar | 31254100PubMed |
Demirevska K, Zasheva D, Dimitrov R, Simova-Stoilova L, Stamenova M, Feller U (2009) Drought stress effects on Rubisco in wheat: changes in the Rubisco large subunit. Acta Physiologiae Plantarum 31, 1129–1138.
| Drought stress effects on Rubisco in wheat: changes in the Rubisco large subunit.Crossref | GoogleScholarGoogle Scholar |
Dillard HR (2019) Global food and nutrition security: from challenges to solutions. Food Security 11, 249–252.
| Global food and nutrition security: from challenges to solutions.Crossref | GoogleScholarGoogle Scholar |
Echeverria E, Salvucci ME, Gonzalez P, Paris G, Salerno G (1997) Physical and kinetic evidence for an association between sucrose-phosphate synthase and sucrose-phosphate phosphatase. Plant Physiology 115, 223–227.
| Physical and kinetic evidence for an association between sucrose-phosphate synthase and sucrose-phosphate phosphatase.Crossref | GoogleScholarGoogle Scholar | 12223802PubMed |
Evans JR, Santiago LS (2014) PrometheusWiki Gold Leaf Protocol: gas exchange using LI-COR 6400. Functional Plant Biology 41, 223–226.
| PrometheusWiki Gold Leaf Protocol: gas exchange using LI-COR 6400.Crossref | GoogleScholarGoogle Scholar | 32480982PubMed |
Fan Y, Zhong Z, Zhang X (2011) Determination of photosynthetic parameters Vcmax and J max for a C3 plant (spring hulless barley) at two altitudes on the Tibetan Plateau. Agricultural and Forest Meteorology 151, 1481–1487.
| Determination of photosynthetic parameters Vcmax and J max for a C3 plant (spring hulless barley) at two altitudes on the Tibetan Plateau.Crossref | GoogleScholarGoogle Scholar |
Furbank RT, Quick WP, Sirault XRR (2015) Improving photosynthesis and yield potential in cereal crops by targeted genetic manipulation: prospects, progress and challenges. Field Crops Research 182, 19–29.
| Improving photosynthesis and yield potential in cereal crops by targeted genetic manipulation: prospects, progress and challenges.Crossref | GoogleScholarGoogle Scholar |
Geber MA, Dawson TE (1997) Genetic variation in stomatal and biochemical limitations to photosynthesis in the annual plant, Polygonum arenastrum. Oecologia 109, 535–546.
| Genetic variation in stomatal and biochemical limitations to photosynthesis in the annual plant, Polygonum arenastrum.Crossref | GoogleScholarGoogle Scholar | 28307337PubMed |
Ho LC, Thornley JHM (1978) Energy requirements for assimilate translocation from mature tomato leaves. Annals of Botany 42, 481–483.
| Energy requirements for assimilate translocation from mature tomato leaves.Crossref | GoogleScholarGoogle Scholar |
Jenner CF, Ugalde TD, Aspinall D (1991) The physiology of starch and protein deposition in the endosperm of wheat. Functional Plant Biology 18, 211–226.
| The physiology of starch and protein deposition in the endosperm of wheat.Crossref | GoogleScholarGoogle Scholar |
Jia S, Lv J, Jiang S, Liang T, Liu C, Jing Z (2015) Response of wheat ear photosynthesis and photosynthate carbon distribution to water deficit. Photosynthetica 53, 95–109.
| Response of wheat ear photosynthesis and photosynthate carbon distribution to water deficit.Crossref | GoogleScholarGoogle Scholar |
Jiang S-Y, Chi Y-H, Wang J-Z, Zhou J-X, Cheng Y-S, Zhang B-L, Ma A, Vanitha J, Ramachandran S (2015) Sucrose metabolism gene families and their biological functions. Scientific Reports 5, 17583
| Sucrose metabolism gene families and their biological functions.Crossref | GoogleScholarGoogle Scholar | 26616172PubMed |
Jiang Y, Guo W, Zhu H, Ruan Y-L, Zhang T (2012) Overexpression of GhSusA1 increases plant biomass and improves cotton fiber yield and quality. Plant Biotechnology Journal 10, 301–312.
| Overexpression of GhSusA1 increases plant biomass and improves cotton fiber yield and quality.Crossref | GoogleScholarGoogle Scholar | 22044435PubMed |
Koch K (2004) Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Current Opinion in Plant Biology 7, 235–246.
| Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development.Crossref | GoogleScholarGoogle Scholar | 15134743PubMed |
Koch KE, Wu Y, Xu J (1996) Sugar and metabolic regulation of genes for sucrose metabolism: potential influence of maize sucrose synthase and soluble invertase responses on carbon partitioning and sugar sensing. Journal of Experimental Botany 1179–1185.
| Sugar and metabolic regulation of genes for sucrose metabolism: potential influence of maize sucrose synthase and soluble invertase responses on carbon partitioning and sugar sensing.Crossref | GoogleScholarGoogle Scholar | 21245246PubMed |
Kubis A, Bar-Even A (2019) Synthetic biology approaches for improving photosynthesis. Journal of Experimental Botany 70, 1425–1433.
| Synthetic biology approaches for improving photosynthesis.Crossref | GoogleScholarGoogle Scholar | 30715460PubMed |
Li Y, Heckmann D, Lercher MJ, Maurino VG (2017) Combining genetic and evolutionary engineering to establish C4 metabolism in C3 plants. Journal of Experimental Botany 68, 117–125.
| Combining genetic and evolutionary engineering to establish C4 metabolism in C3 plants.Crossref | GoogleScholarGoogle Scholar | 27660481PubMed |
Lunn JE, MacRae E (2003) New complexities in the synthesis of sucrose. Current Opinion in Plant Biology 6, 208–214.
| New complexities in the synthesis of sucrose.Crossref | GoogleScholarGoogle Scholar | 12753969PubMed |
Makino A, Mae T, Ohira K (1984) Relation between nitrogen and ribulose-1,5-bisphosphate carboxylase in rice leaves from emergence through senescence. Plant and Cell Physiology 25, 429–437.
| Relation between nitrogen and ribulose-1,5-bisphosphate carboxylase in rice leaves from emergence through senescence.Crossref | GoogleScholarGoogle Scholar |
Makino A, Sakashita H, Hidema J, Mae T, Ojima K, Osmond B (1992) Distinctive responses of ribulose-1,5-bisphosphate carboxylase and carbonic anhydrase in wheat leaves to nitrogen nutrition and their possible relationships to CO2-transfer resistance. Plant Physiology 100, 1737–1743.
| Distinctive responses of ribulose-1,5-bisphosphate carboxylase and carbonic anhydrase in wheat leaves to nitrogen nutrition and their possible relationships to CO2-transfer resistance.Crossref | GoogleScholarGoogle Scholar | 16653191PubMed |
Molero G, Reynolds MP (2020) Spike photosynthesis measured at high throughput indicates genetic variation independent of flag leaf photosynthesis. Field Crops Research 255, 107866
| Spike photosynthesis measured at high throughput indicates genetic variation independent of flag leaf photosynthesis.Crossref | GoogleScholarGoogle Scholar |
Nie G, Hendrix DL, Webber AN, Kimball BA, Long SP (1995) Increased accumulation of carbohydrates and decreased photosynthetic gene transcript levels in wheat grown at an elevated CO2 concentration in the field. Plant Physiology 108, 975–983.
| Increased accumulation of carbohydrates and decreased photosynthetic gene transcript levels in wheat grown at an elevated CO2 concentration in the field.Crossref | GoogleScholarGoogle Scholar | 12228521PubMed |
Nikolau BJ, Klessig DF (1987) Coordinate, organ-specific and developmental regulation of ribulose 1,5-bisphosphate carboxylase gene expression in Amaranthus hypochondriacus. Plant Physiology 85, 167–173.
| Coordinate, organ-specific and developmental regulation of ribulose 1,5-bisphosphate carboxylase gene expression in Amaranthus hypochondriacus.Crossref | GoogleScholarGoogle Scholar | 16665651PubMed |
Paul MJ, Pellny TK (2003) Carbon metabolite feedback regulation of leaf photosynthesis and development. Journal of Experimental Botany 54, 539–547.
| Carbon metabolite feedback regulation of leaf photosynthesis and development.Crossref | GoogleScholarGoogle Scholar | 12508065PubMed |
Poovaiah CR, Mazarei M, Decker SR, Turner GB, Sykes RW, Davis MF, Stewart CN (2015) Transgenic switchgrass (Panicum virgatum L.) biomass is increased by overexpression of switchgrass sucrose synthase (PvSUS1). Biotechnology Journal 10, 552–563.
| Transgenic switchgrass (Panicum virgatum L.) biomass is increased by overexpression of switchgrass sucrose synthase (PvSUS1).Crossref | GoogleScholarGoogle Scholar | 25327983PubMed |
Rajala A, Hakala K, Mäkelä P, Muurinen S, Peltonen-Sainio P (2009) Spring wheat response to timing of water deficit through sink and grain filling capacity. Field Crops Research 114, 263–271.
| Spring wheat response to timing of water deficit through sink and grain filling capacity.Crossref | GoogleScholarGoogle Scholar |
Rangan P, Furtado A, Henry RJ (2016) New evidence for grain specific C4 photosynthesis in wheat. Scientific Reports 6, 31721
| New evidence for grain specific C4 photosynthesis in wheat.Crossref | GoogleScholarGoogle Scholar | 27530078PubMed |
Ruan Y-L, Llewellyn DJ, Furbank RT (2003) Suppression of sucrose synthase gene expression represses cotton fiber cell initiation, elongation, and seed development. The Plant Cell 15, 952–964.
| Suppression of sucrose synthase gene expression represses cotton fiber cell initiation, elongation, and seed development.Crossref | GoogleScholarGoogle Scholar | 12671090PubMed |
Sasaki Y, Nakamura Y, Matsuno R (1987) Regulation of gene expression of ribulose bisphosphate carboxylase in greening pea leaves. Plant Molecular Biology 8, 375–382.
| Regulation of gene expression of ribulose bisphosphate carboxylase in greening pea leaves.Crossref | GoogleScholarGoogle Scholar | 24301259PubMed |
Seneweera S, Makino A, Hirotsu N, Norton R, Suzuki YJE, Botany E (2011) New insight into photosynthetic acclimation to elevated CO2: the role of leaf nitrogen and ribulose-1,5-bisphosphate carboxylase/oxygenase content in rice leaves. Environmental and Experimental Botany 71, 128–136.
| New insight into photosynthetic acclimation to elevated CO2: the role of leaf nitrogen and ribulose-1,5-bisphosphate carboxylase/oxygenase content in rice leaves.Crossref | GoogleScholarGoogle Scholar |
Seneweera SP, Basra AS, Barlow EW, Conroy JP (1995) Diurnal regulation of leaf blade elongation in rice by CO2 : Is it related to sucrose-phosphate synthase activity? Plant Physiology 108, 1471–1477.
| Diurnal regulation of leaf blade elongation in rice by CO2 : Is it related to sucrose-phosphate synthase activity?Crossref | GoogleScholarGoogle Scholar | 12228556PubMed |
Serrago RA, Alzueta I, Savin R, Slafer GA (2013) Understanding grain yield responses to source–sink ratios during grain filling in wheat and barley under contrasting environments. Field Crops Research 150, 42–51.
| Understanding grain yield responses to source–sink ratios during grain filling in wheat and barley under contrasting environments.Crossref | GoogleScholarGoogle Scholar |
Stitt M (1986) Limitation of photosynthesis by carbon metabolism: I. Evidence for excess electron transport capacity in leaves carrying out photosynthesis in saturating light and CO2. Plant Physiology 81, 1115–1122.
| Limitation of photosynthesis by carbon metabolism: I. Evidence for excess electron transport capacity in leaves carrying out photosynthesis in saturating light and CO2.Crossref | GoogleScholarGoogle Scholar | 16664953PubMed |
Stitt M, Lunn J, Usadel B (2010) Arabidopsis and primary photosynthetic metabolism – more than the icing on the cake. The Plant Journal 61, 1067–1091.
| Arabidopsis and primary photosynthetic metabolism – more than the icing on the cake.Crossref | GoogleScholarGoogle Scholar | 20409279PubMed |
Suzuki Y, Kihara-Doi T, Kawazu T, Miyake C, Makino A (2010) Differences in Rubisco content and its synthesis in leaves at different positions in Eucalyptus globulus seedlings. Plant, Cell & Environment 33, 1314–1323.
| Differences in Rubisco content and its synthesis in leaves at different positions in Eucalyptus globulus seedlings.Crossref | GoogleScholarGoogle Scholar |
Suzuki Y, Makino A, Mae T (2001) Changes in the turnover of Rubisco and levels of mRNAs of rbcL and rbcS in rice leaves from emergence to senescence. Plant, Cell & Environment 24, 1353–1360.
| Changes in the turnover of Rubisco and levels of mRNAs of rbcL and rbcS in rice leaves from emergence to senescence.Crossref | GoogleScholarGoogle Scholar |
Suzuki Y, Miyamoto T, Yoshizawa R, Mae T, Makino A (2009) Rubisco content and photosynthesis of leaves at different positions in transgenic rice with an overexpression of RBCS. Plant, Cell & Environment 32, 417–427.
| Rubisco content and photosynthesis of leaves at different positions in transgenic rice with an overexpression of RBCS.Crossref | GoogleScholarGoogle Scholar |
van Bezouw RFHM, Keurentjes JJB, Harbinson J, Aarts MGM (2019) Converging phenomics and genomics to study natural variation in plant photosynthetic efficiency. The Plant Journal 97, 112–133.
| Converging phenomics and genomics to study natural variation in plant photosynthetic efficiency.Crossref | GoogleScholarGoogle Scholar | 30548574PubMed |
Vicente R, Pérez P, Martínez-Carrasco R, Usadel B, Kostadinova S, Morcuende R (2015) Quantitative RT–PCR platform to measure transcript levels of C and N metabolism-related genes in durum wheat: transcript profiles in elevated [CO2] and high temperature at different levels of N supply. Plant and Cell Physiology 56, 1556–1573.
| Quantitative RT–PCR platform to measure transcript levels of C and N metabolism-related genes in durum wheat: transcript profiles in elevated [CO2] and high temperature at different levels of N supply.Crossref | GoogleScholarGoogle Scholar | 26063390PubMed |
Vu JC, Allen LH, Gesch RW (2006) Up-regulation of photosynthesis and sucrose metabolism enzymes in young expanding leaves of sugarcane under elevated growth CO2. Plant Science 171, 123–131.
| Up-regulation of photosynthesis and sucrose metabolism enzymes in young expanding leaves of sugarcane under elevated growth CO2.Crossref | GoogleScholarGoogle Scholar |
Walker AP, Beckerman AP, Gu L, Kattge J, Cernusak LA, Domingues TF, Scales JC, Wohlfahrt G, Wullschleger SD, Woodward FI (2014) The relationship of leaf photosynthetic traits – Vcmax and J max – to leaf nitrogen, leaf phosphorus, and specific leaf area: a meta-analysis and modeling study. Ecology and Evolution 4, 3218–3235.
| The relationship of leaf photosynthetic traits – Vcmax and J max – to leaf nitrogen, leaf phosphorus, and specific leaf area: a meta-analysis and modeling study.Crossref | GoogleScholarGoogle Scholar | 25473475PubMed |
Wang S, Tholen D, Zhu X-G (2017) C4 photosynthesis in C3 rice: a theoretical analysis of biochemical and anatomical factors. Plant, Cell & Environment 40, 80–94.
| C4 photosynthesis in C3 rice: a theoretical analysis of biochemical and anatomical factors.Crossref | GoogleScholarGoogle Scholar |
White JC, Gardea-Torresdey J (2018) Achieving food security through the very small. Nature Nanotechnology 13, 627
| Achieving food security through the very small.Crossref | GoogleScholarGoogle Scholar | 30082813PubMed |
Wullschleger SD (1993) Biochemical limitations to carbon assimilation in C3 plants—a retrospective analysis of the ACi curves from 109 species. Journal of Experimental Botany 44, 907–920.
| Biochemical limitations to carbon assimilation in C3 plants—a retrospective analysis of the ACi curves from 109 species.Crossref | GoogleScholarGoogle Scholar |
Zhang M, Gao Y, Zhang Y, Fischer T, Zhao Z, Zhou X, Wang Z, Wang E (2020) The contribution of spike photosynthesis to wheat yield needs to be considered in process-based crop models. Field Crops Research 257, 107931
| The contribution of spike photosynthesis to wheat yield needs to be considered in process-based crop models.Crossref | GoogleScholarGoogle Scholar |
