Effects of endogenous ascorbic acid on the distribution of photosynthetic electron flow in rice leaves
Qilei Zhang
A , Minling Cai A , Lina Lu A , Hui Gao A and Changlian Peng A B
+ 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 Science, South China Normal University, Guangzhou 510631, P.R. China.
B Corresponding author. Email: pengchl@scib.ac.cn
Crop and Pasture Science 70(10) 849-857 https://doi.org/10.1071/CP19200
Submitted: 3 April 2019 Accepted: 21 July 2019 Published: 18 October 2019
Abstract
Ascorbic acid (Asc) is one of the major antioxidants in plants. l-Galactono-1,4-lactone dehydrogenase (GLDH) is an enzyme that catalyses the last step of Asc biosynthesis in higher plants. In this study the effects of endogenous Asc on the distribution of photosynthetic electron flow were investigated in wild-type (ZH-11) rice (Oryza sativa L.) and in GLDH-overexpressing (GO-2) and GLDH-suppressed (GI-2) transgenic rice. The ratio of photosynthetic electron flow distributed to Rubisco-dependent carboxylation was highest in GO-2, whereas other electron flows in addition to carbon fixation were highest in GI-2 after flowering. Further examination showed that the photosynthetic electron flow, GLDH content and reactive oxygen species-scavenging ability were highest in GO-2 and lowest in GI-2. Therefore, the senescence of leaves was faster in GI-2 but slower in GO-2 compared with ZH-11. In addition, leaves with higher Asc content had more Rubisco content and a superior photosynthetic rate, which increased rice yield. These results suggest that increasing the endogenous Asc content of rice delays senescence, maintains a higher photosynthetic rate and results in more photosynthetic electron flow distributed to Rubisco-dependent carboxylation, ultimately leading to increased rice yield.
Additional keyword: photosynthesis.
References
Ainsworth EA, Long SP (2005) What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytologist 165, 351–372.| What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2.Crossref | GoogleScholarGoogle Scholar | 15720649PubMed |
Akram NA, Shafiq F, Ashraf M (2017) Ascorbic acid – a potential oxidant scavenger and its role in plant development and abiotic stress tolerance. Frontiers in Plant Science 8, 613
| Ascorbic acid – a potential oxidant scavenger and its role in plant development and abiotic stress tolerance.Crossref | GoogleScholarGoogle Scholar | 28491070PubMed |
Barna B, Fodor J, Harrach BD, Pogány M, Király Z (2012) The Janus face of reactive oxygen species in resistance and susceptibility of plants to necrotrophic and biotrophic pathogens. Plant Physiology and Biochemistry 59, 37–43.
| The Janus face of reactive oxygen species in resistance and susceptibility of plants to necrotrophic and biotrophic pathogens.Crossref | GoogleScholarGoogle Scholar | 22321616PubMed |
Barth C, Moeder W, Klessig DF, Conklin PL (2004) The timing of senescence and response to pathogens is altered in the ascorbate-deficient Arabidopsis mutant vitamin c-1. Plant Physiology 134, 1784–1792.
| The timing of senescence and response to pathogens is altered in the ascorbate-deficient Arabidopsis mutant vitamin c-1.Crossref | GoogleScholarGoogle Scholar | 15064386PubMed |
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, 335–344.
| Ascorbate biosynthesis in mitochondria is linked to the electron transport chain between complexes III and IV.Crossref | GoogleScholarGoogle Scholar | 10806250PubMed |
Betti M, Bauwe H, Busch FA, Fernie AR, Keech O, Levey M, Ort DR, Parry MAJ, Sage R, Timm S, Walker B, Weber APM (2016) Manipulating photorespiration to increase plant productivity: recent advances and perspectives for crop improvement. Journal of Experimental Botany 67, 2977–2988.
| Manipulating photorespiration to increase plant productivity: recent advances and perspectives for crop improvement.Crossref | GoogleScholarGoogle Scholar | 26951371PubMed |
Chen Y, Zhang C, Su Y, Ma J, Zhang Z, Yuan M, Zhang H, Yuan S (2017) Responses of photosystem II and antioxidative systems to high light and high temperature co-stress in wheat. Environmental and Experimental Botany 135, 45–55.
| Responses of photosystem II and antioxidative systems to high light and high temperature co-stress in wheat.Crossref | GoogleScholarGoogle Scholar |
Fridman S, Floresuribe J, Larom S, Alalouf O, Liran O, Yacoby I, Salama F, Bailleul B, Rappaport F, Ziv T, Sharon I, Castillo FMC, Philosof A, Dupont CL, Sánchez P, Acinas SG, Rohwer FL, Lindell D, Beja O (2017) A myovirus encoding both photosystem I and II proteins enhances cyclic electron flow in infected prochlorococcus cells. Nature Microbiology 2, 1350–1357.
| A myovirus encoding both photosystem I and II proteins enhances cyclic electron flow in infected prochlorococcus cells.Crossref | GoogleScholarGoogle Scholar | 28785078PubMed |
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 – General ubjects 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 |
Gilbert L, Alhagdow M, Nunes-Nesi A, Quemener B, Guillon F, Bouchet B, Faurobert M, Gouble B, Page D, Garcia V, Petit J, Stevens R, Causse M, Fernie AR, Lahaye M, Rothan C, Baldet P (2009) GDP-d-mannose 3,5-epimerase (GME) plays a key role at the intersection of ascorbate and non-cellulosic cell-wall biosynthesis in tomato. The Plant Journal 60, 499–508.
| GDP-d-mannose 3,5-epimerase (GME) plays a key role at the intersection of ascorbate and non-cellulosic cell-wall biosynthesis in tomato.Crossref | GoogleScholarGoogle Scholar | 19619161PubMed |
Hideg E, Schreiber U (2007) Parallel assessment of ROS formation and photosynthesis in leaves by fluorescence imaging. Photosynthesis Research 92, 103–108.
| Parallel assessment of ROS formation and photosynthesis in leaves by fluorescence imaging.Crossref | GoogleScholarGoogle Scholar | 17486428PubMed |
Hrstka M, Urban O, Babák L (2012) Seasonal changes of Rubisco content and activity in Fagus sylvatica and Picea abies affected by elevated CO2 concentration. Chemical Papers 66, 836–841.
| Seasonal changes of Rubisco content and activity in Fagus sylvatica and Picea abies affected by elevated CO2 concentration.Crossref | GoogleScholarGoogle Scholar |
Huner NP, Öquist G, Sarhan F (1998) Energy balance and acclimation to light and cold. Trends in Plant Science 3, 224–230.
| Energy balance and acclimation to light and cold.Crossref | GoogleScholarGoogle Scholar |
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, Van Motagu M, Inzé 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 |
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 |
Li Z, Wakao S, Fischer BB, Niyogi KK (2009) Sensing and responding to excess light. Annual Review of Plant Biology 60, 239–260.
| Sensing and responding to excess light.Crossref | GoogleScholarGoogle Scholar | 19575582PubMed |
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 |
Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods in Enzymology 148, 350–382.
| Chlorophylls and carotenoids: pigments of photosynthetic biomembranes.Crossref | GoogleScholarGoogle Scholar |
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 |
Liu Y, Yu L, Tong J, Ding J, Wang R, Lu Y, Xiao L (2013) Tiller number is altered in the ascorbic acid-deficient rice suppressed for L-galactono-1,4-lactone dehydrogenase. Journal of Plant Physiology 170, 389–396.
| Tiller number is altered in the ascorbic acid-deficient rice suppressed for L-galactono-1,4-lactone dehydrogenase.Crossref | GoogleScholarGoogle Scholar | 23290459PubMed |
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method. Methods 25, 402–408.
| Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method.Crossref | GoogleScholarGoogle Scholar | 11846609PubMed |
Melis M, Spangfort M, Andersson B (1987) Light-absorption and electron-transport balance between photosystem II and photosystem I in spinach chloroplasts. Photochemistry and Photobiology 45, 129–136.
| Light-absorption and electron-transport balance between photosystem II and photosystem I in spinach chloroplasts.Crossref | GoogleScholarGoogle Scholar |
Müller-Moulé P, Golan T, Niyogi KK (2004) Ascorbate-deficient mutants of Arabidopsis grown in high light despite chronic photooxidative stress. Plant Physiology 134, 1163–1172.
| Ascorbate-deficient mutants of Arabidopsis grown in high light despite chronic photooxidative stress.Crossref | GoogleScholarGoogle Scholar | 14963245PubMed |
Ou Z, Peng C, Lin G, Yang C (2003) Relationship between PSII excitation pressure and content of Rubisco large subunit or small subunit in flag leaf of super high-yielding hybrid rice. Acta Botanica Sinica 45, 929–935.
Oxborough K, Baker NR (1997) Resolving chlorophyll a fluorescence images of photosynthetic efficiency into photochemical and non-photochemical components-calculation of qP and Fv′/Fm′ without measuring Fo′. Photosynthesis Research 54, 135–142.
| Resolving chlorophyll a fluorescence images of photosynthetic efficiency into photochemical and non-photochemical components-calculation of qP and Fv′/Fm′ without measuring Fo′.Crossref | GoogleScholarGoogle Scholar |
Pintó-Marijuan B, 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 |
Potters G, Horemans N, Jansen MAK (2010) The cellular redox state in plant stress biology – a charging concept. Plant Physiology and Biochemistry 48, 292–300.
| The cellular redox state in plant stress biology – a charging concept.Crossref | GoogleScholarGoogle Scholar | 20137959PubMed |
Saha MR, Hasan SMR, Akter R, Hossaina MM, Alamb MS, Alam MA, Mazumderc MEH (2008) In vitro free radical scavenging activity of methanol extract of the leaves of Mimusops elengi Linn. Bangladesh Journal of Veterinary Medicine 6, 197–202.
| In vitro free radical scavenging activity of methanol extract of the leaves of Mimusops elengi Linn.Crossref | GoogleScholarGoogle Scholar |
Schertl P, Sunderhaus S, Klodmann J, Grozeff GE, Bartoli CG, Braun HP (2012) l-Galactono-1,4-lactone dehydrogenase (GLDH) forms part of three subcomplexes of mitochondrial complex I in Arabidopsis thaliana. The Journal of Biological Chemistry 287, 14412–14419.
| l-Galactono-1,4-lactone dehydrogenase (GLDH) forms part of three subcomplexes of mitochondrial complex I in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 22378782PubMed |
Seck PA, Diagne A, Mohanty S, Wopereis MC (2012) Crops that feed the world 7: rice. Food Security 4, 7–24.
| Crops that feed the world 7: rice.Crossref | GoogleScholarGoogle Scholar |
Sedigheh HG, Mortazavian M, Norouzian D, Atyabi M, Akbarzadeh A, Hasanpoor K, Ghorbani M (2011) Oxidative stress and leaf senescence. BMC Research Notes 4, 477
| Oxidative stress and leaf senescence.Crossref | GoogleScholarGoogle Scholar | 22047555PubMed |
Sunil B, Saini D, Bapatla RB, Aswani V, Raghavendra AS (2018) Photorespiration is complemented by cyclic electron flow and the alternative oxidase pathway to optimize photosynthesis and protect against abiotic stress. Photosynthesis Research 139, 67–79.
| Photorespiration is complemented by cyclic electron flow and the alternative oxidase pathway to optimize photosynthesis and protect against abiotic stress.Crossref | GoogleScholarGoogle Scholar | 30187303PubMed |
Taheri P, Irannejad A, Goldani M, Tarighi S (2014) Oxidative burst and enzymatic antioxidant systems in rice plants during interaction with Alternaria alternata. European Journal of Plant Pathology 140, 829–839.
| Oxidative burst and enzymatic antioxidant systems in rice plants during interaction with Alternaria alternata.Crossref | GoogleScholarGoogle Scholar |
Tokunaga T, Miyahara K, Tabata K, Esaka M (2005) Generation and properties of ascorbic acid-overproducing transgenic tobacco cells expressing sense RNA for l-galactono-1,4-lactone dehydrogenase. Planta 220, 854–863.
| Generation and properties of ascorbic acid-overproducing transgenic tobacco cells expressing sense RNA for l-galactono-1,4-lactone dehydrogenase.Crossref | GoogleScholarGoogle Scholar | 15549373PubMed |
Valentini R, Epron D, Angelis PD, Matteucci G, Dreyer E (1995) In situ estimation of net CO2 assimilation, photosynthetic electron flow and photorespiration in Turkey oak (Q. cerris L.) leaves: diural 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: diural cycle under different levels of water supply.Crossref | GoogleScholarGoogle Scholar |
Wada S, Suzuki Y, Takagi D, Miyake C, Makino A (2018) Effects of genetic manipulation of the activity of photorespiration on the redox state of photosystem I and its robustness against excess light stress under CO2-limited conditions in rice. Photosynthesis Research 137, 431–441.
Walker BJ, Vanloocke A, Bernacchi CJ, Ort DR (2016) The costs of photorespiration to food production now and in the future. Annual Review of Plant Biology 67, 107–129.
| The costs of photorespiration to food production now and in the future.Crossref | GoogleScholarGoogle Scholar | 26865340PubMed |
Wawire M, Oey I, Mathooko F, Njoroge C, Shitanda D, Hendrickx M (2011) Thermal stability of ascorbic acid and ascorbic acid oxidase in African cowpea leaves (Vigna unguiculata) of different maturities. Journal of Agricultural and Food Chemistry 59, 1774–1783.
| Thermal stability of ascorbic acid and ascorbic acid oxidase in African cowpea leaves (Vigna unguiculata) of different maturities.Crossref | GoogleScholarGoogle Scholar | 21309563PubMed |
Woo HR, Kim HJ, Nam HG, Lim PO (2013) Plant leaf senescence and death-regulation by multiple layers of control and implications for aging in general. Journal of Cell Science 126, 4823–4833.
| Plant leaf senescence and death-regulation by multiple layers of control and implications for aging in general.Crossref | GoogleScholarGoogle Scholar | 24144694PubMed |
Yu L, Liu Y, Lu L, Zhang Q, Chen Y, Zhou L, Chen H, Peng C (2017) Ascorbic acid deficiency leads to increased grain chalkiness in transgenic rice for suppressed of l-GalLDH. Journal of Plant Physiology 211, 13–26.
| Ascorbic acid deficiency leads to increased grain chalkiness in transgenic rice for suppressed of l-GalLDH.Crossref | GoogleScholarGoogle Scholar | 28142093PubMed |
