Myo-inositol mediates reactive oxygen species-induced programmed cell death via salicylic acid-dependent and ethylene-dependent pathways in apple

Lingyu Hu , Kun Zhou , Guijin Ren , Shulin Yang , Yuan Liu , Zhijun Zhang , Yangtiansu Li , Xiaoqing Gong , Fengwang Ma

Horticulture Research ›› 2020, Vol. 7 ›› Issue (1) : 138

PDF (2257KB)
Horticulture Research ›› 2020, Vol. 7 ›› Issue (1) :138 DOI: 10.1038/s41438-020-00357-2
Article
research-article
Myo-inositol mediates reactive oxygen species-induced programmed cell death via salicylic acid-dependent and ethylene-dependent pathways in apple
Author information +
History +
PDF (2257KB)

Abstract

As a versatile compound, myo-inositol plays vital roles in plant biochemistry and physiology. We previously showed that exogenous application of myo-inositol had a positive role in salinity tolerance in Malus hupehensis Rehd. In this study, we used MdMIPS (the rate-limiting gene of myo-inositol biosynthesis) transgenic apple lines to gain new insights into the physiological role of myo-inositol in apple. Decreasing myo-inositol biosynthesis in apple lines by RNA silencing of MdMIPS1/2 led to extensive programmed cell death, which manifested as necrosis of both the leaves and roots and, ultimately, plant death. Necrosis was directly caused by the excessive accumulation of reactive oxygen species, which may be closely associated with the cell wall polysaccharide-mediated increase in salicylic acid and a compromised antioxidant system, and this process was enhanced by an increase in ethylene production. In addition, a high accumulation of sorbitol promoted necrosis. This synergetic interplay between salicylic acid and ethylene was further supported by the fact that increased myo-inositol accumulation significantly delayed leaf senescence in MdMIPS1-overexpressing apple lines. Taken together, our results indicated that apple myo-inositol regulates reactive oxygen species-induced programmed cell death through salicylic acid-dependent and ethylene-dependent pathways.

Cite this article

Download citation ▾
Lingyu Hu, Kun Zhou, Guijin Ren, Shulin Yang, Yuan Liu, Zhijun Zhang, Yangtiansu Li, Xiaoqing Gong, Fengwang Ma. Myo-inositol mediates reactive oxygen species-induced programmed cell death via salicylic acid-dependent and ethylene-dependent pathways in apple. Horticulture Research, 2020, 7 (1) : 138 DOI:10.1038/s41438-020-00357-2

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Valluru, R. & Van den Ende, W. Myo-inositol and beyond-emerging networks under stress. Plant Sci. 181, 387-400 (2011).

[2]

Van den Ende, W. Multifunctional fructans and raffinose family oligosaccharides. Front. Plant Sci. 4, 247 (2013).

[3]

Taji, T., Takahashi, S. & Shinozaki, K. Inositols and their metabolites in abiotic and biotic stress responses. Subcell. Biochem. 39, 239-264 (2006).

[4]

Zhai, H. et al. A myo-inositol-1-phosphate synthase gene, IbMIPS1, enhances salt and drought tolerance and stem nematode resistance in transgenic sweet potato. Plant Biotechnol. J. 14, 592-602 (2016).

[5]

Wang, W. et al. An inositolphosphorylceramide synthase is involved in regulation of plant programmed cell death associated with defense in Arabidopsis. Plant Cell 20, 3163-3179 (2008).

[6]

Berkey, R., Bendigeri, D. & Xiao, S. Sphingolipids and plant defense/disease: the “death” connection and beyond. Front. Plant Sci. 3, 68 (2012).

[7]

Loewus, F. A. Inositol and plant cell wall polysaccharide biogenesis. Subcell. Biochem. 39, 21-45 (2006).

[8]

Loewus, F. A. & Murthy, P. P. N. Myo-Inositol metabolism in plants. Plant Sci. 150, 1-19 (2000).

[9]

Eisenberg, F., Bolden, A. H. & Loewus, F. A. Inositol formation by cyclization of glucose chain in rat testis. Biochem. Biophys. Res. Commun. 14, 419-424 (1964).

[10]

Majumder, A. L., Chatterjee, A., Ghosh Dastidar, K. & Majee, M. Diversification and evolution of L-myo-inositol 1-phosphate synthase. FEBS Lett. 553, 3-10 (2003).

[11]

Hazra, A., Dasgupta, N., Sengupta, S. & Das, S. MIPS: Functional dynamics in evolutionary pathways of plant kingdom. Genomics 111, 1929-1945 (2019).

[12]

Ghosh Dastidar, K., Chatterjee, A., Chatterjee, A. & Majumder, A. L. Evolutionary divergence of L-myo-inositol 1-phosphate synthase: significance of a “core catalytic structure”. Subcell. Biochem. 39, 315-340 (2006).

[13]

Torabinejad, J. & Gillaspy, G. E. Functional genomics of inositol metabolism. Subcell. Biochem. 39, 47-70 (2006).

[14]

Donahue, J. L. et al. The Arabidopsis thaliana myo-Inositol 1-phosphate synthase1 gene is required for myo-inositol synthesis and suppression of cell death. Plant Cell 22, 888-903 (2010).

[15]

Meng, P. H. et al. Crosstalks between myo-inositol metabolism, programmed cell death and basal immunity in Arabidopsis. PLoS ONE 4, e7364 (2009).

[16]

Luo, Y. et al. D-myo-inositol-3-phosphate affects phosphatidylinositol-mediated endomembrane function in Arabidopsis and is essential for auxin-regulated embryogenesis. Plant Cell 23, 1352-1372 (2011).

[17]

Keller, R., Brearley, C. A., Trethewey, R. N. & Müller-Röber, B. Reduced inositol content and altered morphology in transgenic potato plants inhibited for 1D-myo-inositol-3-phosphate synthase. Plant J. 16, 403-410 (1998).

[18]

van Doorn, W. G. & Woltering, E. J. Senescence and programmed cell death: substance or semantics? J. Exp. Bot. 406, 2147-2215 (2004).

[19]

Williams, B. & Dickman, M. Plant programmed cell death: can’t live with it; can’t live without it. Mol. Plant Pathol. 9, 531-544 (2008).

[20]

Overmyer, K., Brosché, M. & Kangasjärvi, J. Reactive oxygen species and hormonal control of cell death. Trends Plant Sci. 7, 335-342 (2003).

[21]

Malik, B. et al. Plant signaling: response to reactive oxygen species In Plant Signaling: Understanding the Molecular Crosstalk 1-38 (Springer, New Delhi, 2014).

[22]

Sharma, P., Jha, A. B., Dubey, R. S. & Pessarakli, M. Reactive oxgen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J. Bot. 2012, 1-26 (2012).

[23]

Vlot, A. C., Dempsey, D. A. & Klessig, D. F. Salicylic acid, a multifaceted hormone to combat disease. Annu. Rev. Phytopathol. 47, 177-206 (2009).

[24]

Guo, P. et al. A tripartite amplification loop involving the transcription factor WRKY75, salicylic acid, and reactive oxygen species accelerates leaf senescence. Plant Cell 29, 2854-2870 (2017).

[25]

Adams-Phillips, L., Barry, C. & Giovannoni, J. Signal transduction systems regulating fruit ripening. Trends Plant Sci. 9, 331-338 (2004).

[26]

Xu, J. & Zhang, S. Regulation of ethylene biosynthesis and signaling by protein kinases and phosphatases. Mol. Plant 7, 939-942 (2014).

[27]

Fluhr, R., Mattoo, A. K. & Dilley, D. R. Ethylene-biosynthesis and perception. Crit. Rev. Plant Sci. 15, 479-523 (1996).

[28]

Cin, V. D., Danesin, M., Boschetti, A., Dorigoni, A. & Ramina, A. Ethylene biosynthesis and perception in apple fruitlet abscission (Malus domestica L. Borck). J. Exp. Bot. 421, 2995-3005 (2005).

[29]

Joo, S., Liu, Y., Lueth, A. & Zhang, S. MAPK phosphorylation-induced stabilization of ACS6 protein is mediated by the non-catalytic C-terminal domain, which also contains the cis-determinant for rapid degradation by the 26S proteasome pathway. Plant J. 54, 129-140 (2008).

[30]

Christians, M. J. et al. The BTB ubiquitin ligases ETO1, EOL1 and EOL2 act collectively to regulate ethylene biosynthesis in Arabidopsis by controlling type-2 ACC synthase levels. Plant J. 57, 332-345 (2009).

[31]

Xu, H. et al. Transcriptome analysis reveals a regulation of ethylene-induced post-harvest senescence in pear fruit. Sci. Hortic. 240, 585-591 (2018).

[32]

Hu, L. et al. Exogenous myo-inositol alleviates salinity-induced stress in Malus hupehensis Rehd. Plant Physiol. Biochem. 133, 116-126 (2018).

[33]

Velasco, R. et al. The genome of the domesticated apple (Malus × domestica Borkh.). Nat. Genet. 42, 833-839 (2010).

[34]

Basak, P. et al. An evolutionary analysis identifies a conserved pentapeptide stretch containing the two essential lysine residues for rice L-myo-inositol 1-phosphate synthase catalytic activity. PLoS ONE 12, e0185351 (2017).

[35]

Yu, S. W. Cellular and genetic responses of plants to sugar starvation. Plant Physiol. 121, 687-693 (1999).

[36]

Vorwerk, S., Somerville, S. & Somerville, C. The role of plant cell wall polysaccharide composition in disease resistance. Trends Plant Sci. 9, 203-209 (2004).

[37]

Gallego-Giraldo, L., Jikumaru, Y., Kamiya, Y., Tang, Y. & Dixon, R. A. Selective lignin downregulation leads to constitutive defense response expression in alfalfa (Medicago sativa L.). N. Phytol. 190, 627-639 (2011).

[38]

Gallego-Giraldo, L., Escamilla-Trevino, L., Jackson, L. & Dixon, R. A. Salicylic acid mediates the reduced growth of lignin down-regulated plants. Proc. Natl Acad. Sci. USA 20, 20814-20819 (2011).

[39]

Iqbal, N. et al. Ethylene role in plant growth, development and senescence: interaction with other phytohormones. Front. Plant Sci. 8, 475 (2017).

[40]

Yu, Y. B. & Yang, S. F. Auxin-induced ethylene production and its inhibition by aminoethoxyvinyiglycine and cobalt ion. Plant Physiol. 64, 1074-1077 (1979).

[41]

Merritt, F., Kemper, A. & Tallman, G. Inhibitors of ethylene synthesis inhibit auxin-induced stomatal opening in epidermis detached from leaves of Vicia faba L. Plant Cell Physiol. 2, 223-230 (2001).

[42]

Fleet, C. M., Yen, J. Y., Hill, E. A. & Gillaspy, G. E. Co-suppression of AtMIPS demonstrates cooperation of MIPS1, MIPS2 and MIPS3 in maintaining myo-inositol synthesis. Plant Mol. Biol. 97, 253-263 (2018).

[43]

Bruggeman, Q. et al. Involvement of Arabidopsis hexokinase1 in cell death mediated by myo-inositol accumulation. Plant Cell 27, 1801-1814 (2015).

[44]

Ma, L. et al. Arabidopsis FHY3 and FAR1 regulate light-induced myo-inositol biosynthesis and oxidative stress responses by transcriptional activation of MIPS1. Mol. Plant 9, 541-557 (2016).

[45]

Zhou, K. et al. MdUGT88F1-mediated phloridzin biosynthesis regulates apple development and Valsa canker resistance. Plant Physiol. 180, 2290-2305 (2019).

[46]

Di, X., Comila, J. & Takken, F. L. W. Involvement of salicylic acid, ethylene and jasmonic acid signalling pathways in the susceptibility of tomato to Fusarium oxysporum. Mol. Plant Pathol. 18, 1024-1035 (2017).

[47]

Nunes, A. C. et al. RNAi-mediated silencing of the myo-inositol-1-phosphate synthase gene (GmMIPS1) in transgenic soybean inhibited seed development and reduced phytate content. Planta 224, 125-132 (2006).

[48]

Sheveleva, E. V. et al. Sorbitol-6-phosphate dehydrogenase expression in transgenic tobacco. High amounts of sorbitol lead to necrotic lesions. Plant Physiol. 117, 831-839 (1998).

[49]

Murphy, A. M., Otto, B., Brearley, C. A., Carr, J. P. & Hanke, D. E. A role for inositol hexakisphosphate in the maintenance of basal resistance to plant pathogens. Plant J. 56, 638-652 (2008).

[50]

Glazebrook, J . Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43, 205-227 (2005).

[51]

Gepstein, S. et al. Large-scale identification of leaf senescence-associated genes. Plant J. 36, 629-642 (2003).

[52]

Dai, H. et al. Development of a seedling clone with high regeneration capacity and susceptibility to Agrobacterium in apple. Sci. Hortic. 164, 202-208 (2013).

[53]

Zhou, K., Hu, L., Li, P., Gong, X. & Ma, F. Genome-wide identification of glycosyltransferases converting phloretin to phloridzin in Malus species. Plant Sci. 265, 131-145 (2017).

[54]

Sun, X. et al. Improvement of drought tolerance by overexpressing MdATG18a is mediated by modified antioxidant system and activated autophagy in transgenic apple. Plant Biotechnol. J. 16, 545-557 (2018).

[55]

Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254 (1976).

[56]

Dahro, B., Wang, F., Peng, T. & Liu, J. H. PtrA/NINV, an alkaline/neutral invertase gene of Poncirus trifoliata, confers enhanced tolerance to multiple abiotic stresses by modulating ROS levels and maintaining photosynthetic efficiency. BMC Plant Biol. 16, 76 (2016).

[57]

Van Soest, P. J. The use of detergents in the analysis of fibrous feeds: II. A rapid method for the determination of fiber and lignin. J. Assoc. Off. Anal. Chem. 46, 829 (1963).

[58]

Chen, W. et al. Novel integrated method for large-scale detection, identification, and quantification of widely targeted metabolites: application in the study of rice metabolomics. Mol. Plant. 6, 1769-1780 (2013).

[59]

Zhu, Q. et al. Identification of xyloglucan endotransglucosylase/hydrolase genes (XTHs) and their expression in persimmon fruit as influenced by 1-methylcyclopropene and gibberellic acid during storage at ambient temperature. Food Chem. 138, 471-477 (2013).

[60]

Wang, P. et al. Delayed senescence of apple leaves by exogenous melatonin treatment: toward regulating the ascorbate-glutathione cycle. J. Pineal Res. 53, 11-20 (2012).

PDF (2257KB)

0

Accesses

0

Citation

Detail

Sections
Recommended

/