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Contribution of ABA metabolism and ROS generation to sugar starvation-induced senescence of rice leaves

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Abstract

To clarify the relationship of sugar starvation with ABA-induced ROS generation during leaf senescence, the genotype-dependent differences in sugar concentration, endogenous ABA content, and ROS generation as well as their temporal patterns during leaf senescence were investigated by using two rice genotypes, namely, Zhehui7954 and its corresponding mutant with the premature senescence of flag leaves (psf). Meanwhile, the interplay between sugar starvation and ABA metabolism in the induction of leaf senescence was examined using detached leaves. The results showed that the psf mutant differed evidently from its wild type (Zhehui7954) in the temporal pattern of soluble sugar, sucrose and hexose (fructose and glucose) contents during leaf senescence, with the rapidly dropping concentrations of total soluble sugar, and sucrose, and hexose for the senescing leaves of psf mutant. Sugar starvation evidently accelerated leaf senescence and significantly enhanced the ABA concentration and malonaldehyde (MDA) accumulation in detached leaves, while exogenous sugar supply severely suppressed the ABA concentration and ROS level in detached leaves, thereby the delayed leaf senescence for the detached leaves treated by exogenous sugar supply. Correspondingly, ABA biosynthesis inhibitor (NDGA) effectively retarded the sugar starvation-induced leaf senescence, while ABA catabolism inhibitor (DNCZ) obviously accelerated leaf senescence by enhancing the endogenous ABA concentration in senescent leaves. Furthermore, sugar starvation severely repressed the transcripts of several key genes related to ABA biosynthesis and its degradation (NCED1, NCED4, NCED5, ABA8ox2 and ABA8ox3), with the significantly lower amount of their transcriptional expression in the senescent leaves of psf mutant relative to its wild type during leaf senescence. Hence, the disequilibrium between ABA biosynthesis and catabolism was strongly responsible for sugar starvation-induced leaf senescence, which was derived from the suppression of ABA degradation, rather than the enhancement of ABA biosynthesis.

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References

  • Asad MAU, Zakari SA, Zhao Q, Zhou L et al (2019) Abiotic stresses intervene with ABA signaling to induce destructive metabolic pathways leading to death: premature leaf senescence in plants. Int J Mol Sci 20:e256

    Article  PubMed  CAS  Google Scholar 

  • Agüera E, Cabello P, De La Haba P (2010) Induction of leaf senescence by low nitrogen nutrition in sunflower (Helianthus annuus) plants. Physiol Plant 138:256–267

    Article  PubMed  CAS  Google Scholar 

  • Barber J, Andersson B (1992) Too much of a good thing: light can be bad for photosynthesis. Trends Biochem Sci 17:61–66

    Article  CAS  PubMed  Google Scholar 

  • Bolouri-Moghaddam MR, Le Roy K, Xiang L, Rolland F et al (2010) Sugar signalling and antioxidant network connections in plant cells. FEBS J 277:2022–2037

    Article  CAS  PubMed  Google Scholar 

  • Borras L, Maddonni G, Otegui M (2003) Leaf senescence in maize hybrids: plant population, row spacing and kernel set effects. Field Crops Res 82:13–26

    Article  Google Scholar 

  • Brouwer B, Ziolkowska A, Bagard M, Keech O et al (2012) The impact of light intensity on shade-induced leaf senescence. Plant Cell Environ 35:1084–1098

    Article  PubMed  Google Scholar 

  • Chen D, Wang S, Xiong B, Cao B et al (2015) Carbon/nitrogen imbalance associated with drought-induced leaf senescence in Sorghum bicolor. PLoS ONE 10:e0137026

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ciereszko I (2018) Regulatory roles of sugars in plant growth and development. Acta Soc Bot Pol 87:35–83

    Article  CAS  Google Scholar 

  • Dai N, Schaffer A, Petreikov M, Shahak Y et al (1999) Overexpression of Arabidopsis hexokinase in tomato plants inhibits growth, reduces photosynthesis, and induces rapid senescence. Plant Cell 11:1253–1266

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fan J, Chen C, Brlansky R, Gmitter FG et al (2010) Changes in carbohydrate metabolism in Citrus sinensis infected with ‘Candidatus Liberibacter asiaticus’. Plant Pathol 59:1037–1043

    Article  CAS  Google Scholar 

  • Fujiki Y, Yoshikawa Y, Sato T, Inada N et al (2001) Dark-inducible genes from Arabidopsis thaliana are associated with leaf senescence and repressed by sugars. Physiol Plant 111:345–352

    Article  CAS  PubMed  Google Scholar 

  • Han C, Kim S, Lee S, Choi S et al (2018) Cross-talk between ABA and sugar signaling is mediated by the ACGT core and CE1 element reciprocally in OsTIP3; 1 promoter. J Plant Physiol 224:103–111

    Article  PubMed  CAS  Google Scholar 

  • Hoeberichts FA, Van Doorn WG, Vorst O, Halz RD et al (2007) Sucrose prevents up-regulation of senescence-associated genes in carnation petals. J Exp Bot 58:2873–2885

    Article  CAS  PubMed  Google Scholar 

  • Ikegami K, Okamoto M, Seo M, Koshiba T (2009) Activation of abscisic acid biosynthesis in the leaves of Arabidopsis thaliana in response to water deficit. J Plant Res 122:235

    Article  CAS  PubMed  Google Scholar 

  • Jiang M, Zhang J (2001) Effect of abscisic acid on active oxygen species, antioxidative defense system and oxidative damage in leaves of maize seedlings. Plant Cell Physiol 42:1265–1273

    Article  CAS  PubMed  Google Scholar 

  • Kojima M, Kamada NT, Komatsu H, Takei K et al (2009) Highly sensitive and high-throughput analysis of plant hormones using MS-probe modification and liquid chromatography–tandem mass spectrometry: an application for hormone profiling in Oryza sativa. Plant Cell Physiol 50:1201–1214

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kukavica B, Jovanovic V (2004) Senescence-related changes in the antioxidant status of ginkgo and birch leaves during autumn yellowing. Physiol Plant 122:321–327

    Article  CAS  Google Scholar 

  • Laby RJ, Kincaid MS, Kim D, Gibson SI (2000) The Arabidopsis sugar-insensitive mutants sis4 and sis5 are defective in abscisic acid synthesis and response. Plant J 23:587–596

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Zhao Q, Cheng F (2020) Sugar starvation enhances leaf senescence and genes involved in sugar signaling pathways regulate early leaf senescence in mutant rice. Rice Sci 27:201–214

    Article  Google Scholar 

  • Liebsch D, Keech O (2016) Dark-induced leaf senescence: new insights into a complex light-dependent regulatory pathway. New Phytol 212:563–570

    Article  CAS  PubMed  Google Scholar 

  • Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382

    Article  CAS  Google Scholar 

  • Lv X, Zhang Y, Fan S, Kong L (2020) Source-sink modifications affect leaf senescence and grain mass in wheat as revealed by proteomic analysis. BMC Plant Biol 20:257–274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mega R, Meguro-Maoka A, Endo A, Shimosaka E et al (2015) Sustained low abscisic acid levels increase seedling vigor under cold stress in rice (Oryza sativa L.). Sci Rep 5:13819–13819

    Article  PubMed  PubMed Central  Google Scholar 

  • Morita-Yamamuro C, Vernieri P, Yamaguchi J (2004) Low sugar status promotes endogenous ABA level and ABA sensitivity in Arabidopsis. Plant Bitechnol 21:9–14

    Article  Google Scholar 

  • Nambara E, Marion-Poll A (2005) Abscisic acid biosynthesis and catabolism. Annu Rev Plant Biol 56:165–185

    Article  CAS  PubMed  Google Scholar 

  • Ono K, Nishi Y, Watanabe A, Terashima I (2001) Possible mechanisms of adaptive leaf senescence. Plant Biol 3:234–243

    Article  CAS  Google Scholar 

  • Pourtau N, Marès M, Purdy S, Quentin N et al (2004) Interactions of abscisic acid and sugar signaling in the regulation of leaf senescence. Planta 219:765–772

    Article  CAS  PubMed  Google Scholar 

  • Qiu C, Ethier G, Pepin S, Dubé P et al (2017) Persistent negative temperature response of mesophyll conductance in red raspberry (Rubus idaeus L.) leaves under both high and low vapour pressure deficits: A role for abscisic acid? Plant Cell Environ 40:1940–1959

    Article  CAS  PubMed  Google Scholar 

  • Rao X, Huang X, Zhou Z, Lin X (2013) An improvement of the 2^(-delta delta CT) method for quantitative real-time polymerase chain reaction data analysis. Biostat Bioinform Biomath 3:71–85

    Google Scholar 

  • Ruan YL, Jin Y, Huang J (2009) Capping invertase activity by its inhibitor: roles and implications in sugar signaling, carbon allocation, senescence and evolution. Plant Signal Behav 4:983–985

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saika H, Okamoto M, Miyoshi K, Kushiro T et al (2007) Ethylene promotes submergence-induced expression of OsABA8ox1, a gene that encodes ABA 8′-hydroxylase in rice. Plant Cell Physiol 48:287–298

    Article  CAS  PubMed  Google Scholar 

  • Song Y, Xiang F, Zhang G, Miao Y et al (2016) Abscisic acid as an internal integrator of multiple physiological processes modulates leaf senescence onset in Arabidopsis thaliana. Front Plant Sci 7:181

    PubMed  PubMed Central  Google Scholar 

  • Srivalli S, Khanna-Chopra R (2009) Delayed wheat flag leaf senescence due to removal of spikelets is associated with increased activities of leaf antioxidant enzymes, reduced glutathione/oxidized glutathione ratio and oxidative damage to mitochondrial proteins. Plant Physiol Biochem 47:663–670

    Article  CAS  PubMed  Google Scholar 

  • Toh S, Imamura A, Watanabe A, Nakabayashi K et al (2008) High temperature-induced abscisic acid biosynthesis and its role in the inhibition of gibberellin action in Arabidopsis seeds. Plant Physiol 146:1368–1385

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang F, Liu J, Chen M, Zhou L et al (2016a) Involvement of abscisic acid in PSII photodamage and D1 protein turnover for light-induced premature senescence of rice flag leaves. PLoS ONE 11:e0161203

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang F, Liu J, Zhou L, Pan G et al (2016b) Senescence-specific change in ROS scavenging enzyme activities and regulation of various SOD isozymes to ROS levels in psf mutant rice leaves. Plant Physiol Biochem 109:248–261

    Article  CAS  PubMed  Google Scholar 

  • Weaver LM, Amasino RM (2001) Senescence is induced in individually darkened Arabidopsis leaves, but inhibited in whole darkened plants. Plant Physiol 127:876–886

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wingler A, Masclaux-Daubresse C, Fischer AM (2009) Sugars, senescence, and ageing in plants and heterotrophic organisms. J Exp Bot 60:1063–1066

    Article  CAS  PubMed  Google Scholar 

  • Wingler A, Purdy S, MacLean JA et al (2005) The role of sugars in integrating environmental signals during the regulation of leaf senescence. J Exp Bot 57:391–399

    Article  PubMed  CAS  Google Scholar 

  • Wingler A, Roitsch T (2008) Metabolic regulation of leaf senescence: interactions of sugar signaling with biotic and abiotic stress responses. Plant Biol 10:50–62

    Article  CAS  PubMed  Google Scholar 

  • Woo HR, Kim HJ, Lim PO, Nam HG (2019) Leaf senescence: systems and dynamics aspects. Annu Rev Plant Biol 70:347–376

    Article  CAS  PubMed  Google Scholar 

  • Xiao S, Gao W, Chen QF, Chan SW et al (2010) Overexpression of Arabidopsis acyl-CoA binding protein ACBP3 promotes starvation-induced and age-dependent leaf senescence. Plant Cell 22:1463–1482

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang J, Zhang J, Wang Z, Zhu Q et al (2003) Involvement of abscisic acid and cytokinins in the senescence and remobilization of carbon reserves in wheat subjected to water stress during grain filling. Plant Cell Environ 26:1621–1631

    Article  CAS  Google Scholar 

  • Yoshida S, Ito M, Nishida I, Watanabe A (2002) Identification of a novel gene HYS1/CPR5 that has a repressive role in the induction of leaf senescence and pathogen-defence responses in Arabidopsis thaliana. Plant J 29:427–437

    Article  CAS  PubMed  Google Scholar 

  • Zhu G, Ye N, Zhang J (2009) Glucose-induced delay of seed germination in rice is mediated by the suppression of ABA catabolism rather than an enhancement of ABA biosynthesis. Plant Cell Physiol 50:644–651

    Article  CAS  PubMed  Google Scholar 

  • Zakari SA, Asad MAU, Han Z, Zhao Q et al (2020) Relationship of nitrogen deficiency-induced leaf senescence with ROS generation and ABA concentration in rice flag leaves. J Plant Growth 39:1503–1517

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors are deeply indebted to National Natural Science Foundation of China (No. 31871566 and 31971819) and National Key Research and Development Plan of China (No 2017YFD0300103) for its financial support to this research project.

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Authors and Affiliations

  1. Institute of Crop Science, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, 310058, China

    Muhmmad Asad Ullah Asad, Fubiao Wang, Yu Ye, Xianyue Guan, Lujian Zhou, Zhanyu Han, Gang Pan & Fangmin Cheng

  2. Research Center for Jinggangshan Eco-Environmental Sciences, Jinggangshan University, Ji’an, 343009, China

    Fubiao Wang

  3. Jiangsu Collaborative Innovation Centre for Modern Crop Production, Nanjing, China

    Fangmin Cheng

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  1. Muhmmad Asad Ullah Asad
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  2. Fubiao Wang
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  3. Yu Ye
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  5. Lujian Zhou
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  6. Zhanyu Han
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  7. Gang Pan
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  8. Fangmin Cheng
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Contributions

Conceived and designed the experiments: MAUA, FW and FC. Performed the experiments: MAUA FW, ZH, XG and LZ. Analyzed the data: MAU, FW, YY and ZH. Wrote the paper: MAU, FC, PG and WF. All of the authors reviewed the manuscript. All authors read and approved the final manuscript.

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Correspondence to Fangmin Cheng.

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Communicated by Hong-Xia Zhang.

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Asad, M.A.U., Wang, F., Ye, Y. et al. Contribution of ABA metabolism and ROS generation to sugar starvation-induced senescence of rice leaves. Plant Growth Regul 95, 241–257 (2021). https://doi.org/10.1007/s10725-021-00718-4

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  • DOI: https://doi.org/10.1007/s10725-021-00718-4

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