The role of ascorbic acid in rice leaf senescence and photo–carbon imbalance
Le Yu
A B , Qilei Zhang A , Lina Lu A , Hui Gao A , Qiang Liu A , Yonghai Liu B , Chengwei Yang A and Changlian Peng A C
+ Author Affiliations
- Author Affiliations
A Guangdong Provincial Key Laboratory of Biotechnology for Plant Development, Guangzhou Key Laboratory of Subtropical Biodiversity and Biomonitoring, College of Life Sciences, South China Normal University, 510631, Guangzhou, China.
B College of Life Sciences, Zhaoqing University, Zhaoqing, 526061, China.
C Corresponding author. Email: pengchl@scib.ac.cn
Functional Plant Biology 47(3) 263-278 https://doi.org/10.1071/FP19248
Submitted: 23 August 2019 Accepted: 18 November 2019 Published: 7 February 2020
Abstract
Leaf senescence is an important factor that affects crop yield traits and is regulated by various factors. Here, we propose the photo–carbon imbalance hypothesis to explain the mechanism of rice leaf senescence. The main idea of this hypothesis is that carbon assimilation decreases faster than the absorption of light energy in photosynthesis during the late stages of rice growth, which ultimately results in leaf senescence. Our results indicate that endogenous ascorbic acid (Asc) plays an important role in leaf senescence by affecting the expression of senescence genes, thereby influencing photosynthetic capacity and consequently grain yield. The effects of exogenous Asc and methyl jasmonate (MeJA) on photosynthetic capability implied that the balance between photoreaction and carbon assimilation is regulated by exogenous antioxidants or accelerators of senescence. The results of the shading treatments indicated that shading will mitigate the photo–carbon imbalance and improve photosynthetic capacity, resulting in increased yields. Increasing antioxidant concentrations can enhance the reactive oxygen species (ROS) scavenging capacity, whereas shading reduces excess light energy, which may help to restore the photo–carbon balance.
Additional keywords: ascorbic acid, photosynthesis, senescence, yield.
References
Amin AA, Rashad ESM, Fatma , Gharib AE (2008) Changes in morphological, physiological and reproductive characters of wheat plants as affected by foliar application with salicylic acid and ascorbic acid. Australian Journal of Basic and Applied Sciences 2, 252–261.Arnon D (1949) Copper enzymes in isolated chloroplasts. Polyphenol oxidase in Beta vulgaris. Plant Physiology 24, 1–15.
| Copper enzymes in isolated chloroplasts. Polyphenol oxidase in Beta vulgaris.Crossref | GoogleScholarGoogle Scholar | 16654194PubMed |
Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiology 141, 391–396.
| Production and scavenging of reactive oxygen species in chloroplasts and their functions.Crossref | GoogleScholarGoogle Scholar | 16760493PubMed |
Bartoli CG, Pastori GM, Foyer CH (2000) Ascorbate biosynthesis in mitochondria is linked to the electron transport chain between complexes III and IV. Plant Physiology 123, 335–343.
| Ascorbate biosynthesis in mitochondria is linked to the electron transport chain between complexes III and IV.Crossref | GoogleScholarGoogle Scholar | 10806250PubMed |
Becker MG, Chan A, Mao X, Girard IJ, Lee S, Elhiti M, Stasolla C, Belmonte MF (2014) Vitamin C deficiency improves somatic embryo development through distinct gene regulatory networks in Arabidopsis. Journal of Experimental Botany 65, 5903–5918.
| Vitamin C deficiency improves somatic embryo development through distinct gene regulatory networks in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 25151615PubMed |
Bryant J, Chapin F, Klein D (1983) Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40, 357–368.
| Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory.Crossref | GoogleScholarGoogle Scholar |
Buchanan-Wollaston V (1997) The molecular biology of leaf senescence. Journal of Experimental Botany 48, 181–199.
| The molecular biology of leaf senescence.Crossref | GoogleScholarGoogle Scholar |
Delpierre N, Dufrêne E, Soudani K, Ulrich E, Cecchini S, Boé J, François C (2009) Modelling interannual and spatial variability of leaf senescence for three deciduous tree species in France. Agricultural and Forest Meteorology 149, 938–948.
| Modelling interannual and spatial variability of leaf senescence for three deciduous tree species in France.Crossref | GoogleScholarGoogle Scholar |
Demmig-Adams B, Cohu CM, Muller O, Adams WW (2012) Modulation of photosynthetic energy conversion efficiency in nature: from seconds to seasons. Photosynthesis Research 113, 75–88.
| Modulation of photosynthetic energy conversion efficiency in nature: from seconds to seasons.Crossref | GoogleScholarGoogle Scholar | 22790560PubMed |
Epron D, Godard D, Cornic G, Genty B (1995) Limitation of net CO2 assimilation rate by internal resistance to CO2 transfer in the leaves of two tree species (Fagus sylvatica L. and Castanea sativa Mill.). Plant, Cell & Environment 18, 43–51.
| Limitation of net CO2 assimilation rate by internal resistance to CO2 transfer in the leaves of two tree species (Fagus sylvatica L. and Castanea sativa Mill.).Crossref | GoogleScholarGoogle Scholar |
Foyer CH, Noctort G (2005) Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant, Cell & Environment 28, 1056–1071.
| Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context.Crossref | GoogleScholarGoogle Scholar |
Gallie DR (2013) The role of L-ascorbic acid recycling in responding to environmental stress and in promoting plant growth. Journal of Experimental Botany 64, 433–443.
| The role of L-ascorbic acid recycling in responding to environmental stress and in promoting plant growth.Crossref | GoogleScholarGoogle Scholar | 23162122PubMed |
Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta 990, 87–92.
| The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence.Crossref | GoogleScholarGoogle Scholar |
Gest N, Gautier H, Stevens R (2013) Ascorbate as seen through plant evolution: the rise of a successful molecule? Journal of Experimental Botany 64, 33–53.
| Ascorbate as seen through plant evolution: the rise of a successful molecule?Crossref | GoogleScholarGoogle Scholar | 23109712PubMed |
Gregersen PL, Holm PB, Krupinska K (2008) Leaf senescence and nutrient remobilisation in barley and wheat. Plant Biology 10, 37–49.
| Leaf senescence and nutrient remobilisation in barley and wheat.Crossref | GoogleScholarGoogle Scholar | 18721310PubMed |
Gregoriou K, Pontikis K, Vemmos S (2007) Effects of reduced irradiance on leaf morphology, photosynthetic capacity, and fruit yield in olive (Olea europaea L.). Photosynthetica 45, 172–181.
| Effects of reduced irradiance on leaf morphology, photosynthetic capacity, and fruit yield in olive (Olea europaea L.).Crossref | GoogleScholarGoogle Scholar |
Harbinson J, Genty B, Baker NR (1990) The relationship between CO2 assimilation and electron transport in leaves. Photosynthesis Research 25, 213–224.
| The relationship between CO2 assimilation and electron transport in leaves.Crossref | GoogleScholarGoogle Scholar | 24420351PubMed |
He Y, Fukushige H, Hildebrand DF, Gan S (2002) Evidence supporting a role of jasmonic acid in Arabidopsis leaf senescence. Plant Physiology 128, 876–884.
| Evidence supporting a role of jasmonic acid in Arabidopsis leaf senescence.Crossref | GoogleScholarGoogle Scholar | 11891244PubMed |
Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Quarterly Review of Biology 67, 283–335.
| The dilemma of plants: to grow or defend.Crossref | GoogleScholarGoogle Scholar |
Höller S, Ueda Y, Wu L, Wang Y, Hajirezaei MR, Ghaffari MR, von Wiren N, Frei M (2015) Ascorbate biosynthesis and its involvement in stress tolerance and plant development in rice (Oryza sativa L.). Plant Molecular Biology 88, 545–560.
| Ascorbate biosynthesis and its involvement in stress tolerance and plant development in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 26129988PubMed |
Jafar MZ, Farooq M, Cheema MA, Afzal I, Basra SMA, Wahid MA, Aziz T, Shahid M (2012) Improving the performance of wheat by seed priming under saline conditions. Journal Agronomy & Crop Science 198, 38–45.
| Improving the performance of wheat by seed priming under saline conditions.Crossref | GoogleScholarGoogle Scholar |
Jiang H, Chen Y, Li M, Xu X, Wu G (2011) Overexpression of SGR results in oxidative stress and lesion-mimic cell death in rice seedlings. Journal of Integrative Plant Biology 53, 375–387.
| Overexpression of SGR results in oxidative stress and lesion-mimic cell death in rice seedlings.Crossref | GoogleScholarGoogle Scholar | 21375689PubMed |
Jochum GM, Mudge KW, Thomas RB (2007) Elevated temperatures increase leaf senescence and root secondary metabolite concentrations in the understory herb Panax quinquefolius (araliaceae). American Journal of Botany 94, 819–826.
| Elevated temperatures increase leaf senescence and root secondary metabolite concentrations in the understory herb Panax quinquefolius (araliaceae).Crossref | GoogleScholarGoogle Scholar | 21636451PubMed |
Juvany M, Müller M, Munné-Bosch S (2013) Photo-oxidative stress in emerging and senescing leaves: a mirror image? Journal of Experimental Botany 64, 3087–3098.
| Photo-oxidative stress in emerging and senescing leaves: a mirror image?Crossref | GoogleScholarGoogle Scholar | 23825233PubMed |
Kampfenkel K, Motagu M, Inzè D (1995) Extraction and determination of ascorbate and dehydroascorbate from plant tissue. Analytical Biochemistry 225, 165–167.
| Extraction and determination of ascorbate and dehydroascorbate from plant tissue.Crossref | GoogleScholarGoogle Scholar | 7778771PubMed |
Kim EH, Kim YS, Park SH, Koo YJ, Choi YD, Chung YY, Lee IJ, Kim JK (2009) Methyl jasmonate reduces grain yield by mediating stress signals to alter spikelet development in rice. Plant Physiology 149, 1751–1760.
| Methyl jasmonate reduces grain yield by mediating stress signals to alter spikelet development in rice.Crossref | GoogleScholarGoogle Scholar | 19211695PubMed |
Krall JP, Edwards GE (1992) Relationship between photosystem II activity and CO2 fixation in leaves. Physiologia Plantarum 86, 180–187.
| Relationship between photosystem II activity and CO2 fixation in leaves.Crossref | GoogleScholarGoogle Scholar |
Lee RH, Wang CH, Huang LT, Chen SC (2001) Leaf senescence in rice plants: cloning and characterization of senescence up-regulated genes. Journal of Experimental Botany 52, 1117–1121.
| Leaf senescence in rice plants: cloning and characterization of senescence up-regulated genes.Crossref | GoogleScholarGoogle Scholar | 11432928PubMed |
Liang C, Wang Y, Zhu Y, Tang J, Hu B, Liu L, Ou S, Wu H, Sun X, Chu J, Chu C (2014) OsNAP connects abscisic acid and leaf senescence by fine-tuning abscisic acid biosynthesis and directly targeting senescence-associated genes in rice. Proceedings of the National Academy of Sciences of the United States of America 111, 10013–10018.
| OsNAP connects abscisic acid and leaf senescence by fine-tuning abscisic acid biosynthesis and directly targeting senescence-associated genes in rice.Crossref | GoogleScholarGoogle Scholar | 24951508PubMed |
Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annual Review of Plant Biology 58, 115–136.
| Leaf senescence.Crossref | GoogleScholarGoogle Scholar | 17177638PubMed |
Lin ZF, Peng CL, Sun ZJ (2000) Effect of light intensity on partitioning of photosynthetic electron transport to photorespiration in four subtropical forest plants. Science China. Life Sciences 43, 347–354.
| Effect of light intensity on partitioning of photosynthetic electron transport to photorespiration in four subtropical forest plants.Crossref | GoogleScholarGoogle Scholar |
Liu Y, Peng X, Li M (2000) Degradation of ribulose-1,5-bisphosphate carboxylase/oxygenase in rice leaves under oxidative stress induced by methyl viologen. Acta Phytophysiologica Sinica 26, 481–486.
Liu Y, Yu L, Wang R (2011) Level of ascorbic acid in transgenic rice for L-galactono-1,4-lactone dehydrogenase overexpressing or suppressed is associated with plant growth and seed set. Acta Physiologiae Plantarum 33, 1353–1363.
| Level of ascorbic acid in transgenic rice for L-galactono-1,4-lactone dehydrogenase overexpressing or suppressed is associated with plant growth and seed set.Crossref | GoogleScholarGoogle Scholar |
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔC(T) Method. Methods 25, 402–408.
| Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔC(T) Method.Crossref | GoogleScholarGoogle Scholar | 11846609PubMed |
Lorence A, Chevone BI, Mendes P, Nessler CL (2004) Myo-inositol oxygenase offers a possible entry point into plant ascorbate biosynthesis. Plant Physiology 134, 1200–1205.
| Myo-inositol oxygenase offers a possible entry point into plant ascorbate biosynthesis.Crossref | GoogleScholarGoogle Scholar | 14976233PubMed |
Mo Z, Li W, Pan S, Fitzgerald TL, Xiao F, Tang Y, Wang Y, Duan M, Tian H, Tang X (2015) Shading during the grain filling period increases 2-acetyl-1-pyrroline content in fragrant rice. Rice 8, 9
| Shading during the grain filling period increases 2-acetyl-1-pyrroline content in fragrant rice.Crossref | GoogleScholarGoogle Scholar | 25844114PubMed |
Müller-Moulé P, Havaux M, Niyogi KK (2003) Zeaxanthin deficiency enhances the high light sensitivity of an ascorbate-deficient mutant of Arabidopsis. Plant Physiology 133, 748–760.
| Zeaxanthin deficiency enhances the high light sensitivity of an ascorbate-deficient mutant of Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 12972657PubMed |
Müller-Moulé P, Golan T, Niyogi KK (2004) Ascorbate-deficient mutants of Arabidopsis grow in high light despite chronic photooxidative stress. Plant Physiology 134, 1163–1172.
| Ascorbate-deficient mutants of Arabidopsis grow in high light despite chronic photooxidative stress.Crossref | GoogleScholarGoogle Scholar | 14963245PubMed |
Munné-Bosch S, Alegre L (2002) Plant aging increases oxidative stress in chloroplasts. Planta 214, 608–615.
| Plant aging increases oxidative stress in chloroplasts.Crossref | GoogleScholarGoogle Scholar | 11925044PubMed |
Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annual Review of Plant Biology 49, 249–279.
| Ascorbate and glutathione: keeping active oxygen under control.Crossref | GoogleScholarGoogle Scholar |
Pinto-Marijuan M, Munné-Bosch S (2014) Photo-oxidative stress markers as a measure of abiotic stress-induced leaf senescence: advantages and limitations. Journal of Experimental Botany 65, 3845–3857.
| Photo-oxidative stress markers as a measure of abiotic stress-induced leaf senescence: advantages and limitations.Crossref | GoogleScholarGoogle Scholar | 24683180PubMed |
Quirino BF, Noh YS, Himelblau E, Amasino RM (2000) Molecular aspects of leaf senescence. Trends in Plant Science 5, 278–282.
| Molecular aspects of leaf senescence.Crossref | GoogleScholarGoogle Scholar | 10871899PubMed |
Schippers JH, Schmidt R, Wagstaff C, Jing HC (2015) Living to die and dying to live: the survival strategy behind leaf senescence. Plant Physiology 169, 914–930.
| Living to die and dying to live: the survival strategy behind leaf senescence.Crossref | GoogleScholarGoogle Scholar | 26276844PubMed |
Sharkey TD (1988) Estimating the rate of photorespiration in leaves. Physiologia Plantarum 73, 147–152.
| Estimating the rate of photorespiration in leaves.Crossref | GoogleScholarGoogle Scholar |
Smirnoff N (2000) Ascorbate biosynthesis and function in photoprotection. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 355, 1455–1464.
| Ascorbate biosynthesis and function in photoprotection.Crossref | GoogleScholarGoogle Scholar | 11127999PubMed |
Smirnoff N, Conklin PL, Loewus FA (2001) Biosynthesis of ascorbic acid in plants: a renaissance. Annual Review of Plant Biology 52, 437–467.
| Biosynthesis of ascorbic acid in plants: a renaissance.Crossref | GoogleScholarGoogle Scholar |
Sun B, Zhou Y, Lin Y (2013) Preliminary functional analysis of a rice leaf senescence up-regulated gene. Zuo Wu Xue Bao 38, 1988–1996.
| Preliminary functional analysis of a rice leaf senescence up-regulated gene.Crossref | GoogleScholarGoogle Scholar |
Tamaoki M, Mukai F, Asai N, Nakajima N, Kubo A, Aono M, Saji H (2003) Light-controlled expression of a gene encoding L-galactono-γ-lactone dehydrogenase which affects ascorbate pool size in Arabidopsis thaliana. Plant Science 164, 1111–1117.
| Light-controlled expression of a gene encoding L-galactono-γ-lactone dehydrogenase which affects ascorbate pool size in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
Valentini R, Epron D, De Angelis P, Matteucci G, Dreyer E (1995) In situ estimation of net CO2 assimilation, photosynthetic electron flow and photorespiration in Turkey oak (Q. cerris L.) leaves: diurnal cycle under different levels of water supply. Plant, Cell & Environment 18, 631–640.
| In situ estimation of net CO2 assimilation, photosynthetic electron flow and photorespiration in Turkey oak (Q. cerris L.) leaves: diurnal cycle under different levels of water supply.Crossref | GoogleScholarGoogle Scholar |
Valpuesta V, Botella MA (2004) Biosynthesis of L-ascorbic acid in plants: new pathways for an old antioxidant. Trends in Plant Science 9, 573–577.
| Biosynthesis of L-ascorbic acid in plants: new pathways for an old antioxidant.Crossref | GoogleScholarGoogle Scholar | 15564123PubMed |
van Doorn WG (2008) Is the onset of senescence in leaf cells of intact plants due to low or high sugar levels? Journal of Experimental Botany 59, 1963–1972.
| Is the onset of senescence in leaf cells of intact plants due to low or high sugar levels?Crossref | GoogleScholarGoogle Scholar | 18453532PubMed |
Wang X, Xu Q, Yang Z (2005) Advances of research on rice leaf senescence physiology. Zhongguo Nongxue Tongbao 21, 187–190, 210.
Wang L, Deng F, Ren WJ, Yang WY (2013) Effects of shading on starch pasting characteristics of Indica hybrid rice (Oryza sativa L.). PLoS One 8, e68220
| Effects of shading on starch pasting characteristics of Indica hybrid rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 24416094PubMed |
Wolucka BA, Van Montagu M (2003) GDP-mannose 3′,5′-epimerase forms GDP-L-gulose, a putative intermediate for the de novo biosynthesis of vitamin C in plants. Journal of Biological Chemistry 278, 47483–47490.
| GDP-mannose 3′,5′-epimerase forms GDP-L-gulose, a putative intermediate for the de novo biosynthesis of vitamin C in plants.Crossref | GoogleScholarGoogle Scholar | 12954627PubMed |
Wu CY, Trieu A, Radhakrishnan P, Kwok SF, Harris S, Zhang K, Wang J, Wan J, Zhai H, Takatsuto S, Matsumoto S, Fujioka S, Feldmann KA, Pennell RI (2008) Brassinosteroids regulate grain filling in rice. The Plant Cell 20, 2130–2145.
| Brassinosteroids regulate grain filling in rice.Crossref | GoogleScholarGoogle Scholar | 18708477PubMed |
Yabuta Y, Mieda T, Rapolu M, Nakamura A, Motoki T, Maruta T, Yoshimura K, Ishikawa T, Shigeoka S (2007) Light regulation of ascorbate biosynthesis is dependent on the photosynthetic electron transport chain but independent of sugars in Arabidopsis. Journal of Experimental Botany 58, 2661–2671.
| Light regulation of ascorbate biosynthesis is dependent on the photosynthetic electron transport chain but independent of sugars in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 17586607PubMed |
Yoshida K (2003) Molecular regulation of leaf senescence. Current Opinion in Plant Biology 6, 79–84.
| Molecular regulation of leaf senescence.Crossref | GoogleScholarGoogle Scholar |
Yu L, Jiang J, Zhang C, Jiang L, Ye N, Lu Y, Yang G, Liu E, Peng C, He Z, Peng X (2010) Glyoxylate rather than ascorbate is an efficient precursor for oxalate biosynthesis in rice. Journal of Experimental Botany 61, 1625–1634.
| Glyoxylate rather than ascorbate is an efficient precursor for oxalate biosynthesis in rice.Crossref | GoogleScholarGoogle Scholar | 20194922PubMed |
Zentgraf U, Hemleben V (2008) Molecular cell biology: are reactive oxygen species regulators of leaf senescence? In ‘Progress in botany. Vol. 69’. (Eds U Lüttge, W Beyschlag, J Murata) pp. 117–138. (Springer: Berlin)
Zhang R, Lin Z (2000) Photosynthetic declination. In ‘Current biology.’ (Ed C Zou) pp. 135–136. (Zhigong Press: Beijing)
Zimmermann P, Zentgraf U (2005) The correlation between oxidative stress and leaf senescence during plant development. Cellular & Molecular Biology Letters 10, 515–534.
