Abstract
Autophagy is a conserved self-degradation process in eukaryotic cells. The execution of autophagy relies on a number of AuTophaGy-related (ATG) factors including ATG8 which is encoded in higher eukaryotes by a family of genes. A protective role of autophagy against environmental stresses has been described in several plant species but not in wheat (Triticum aestivum L.), and information on the functional differentiation of ATG8 family is lacking. In this study, we investigated the responses of wheat autophagy and ATG8 family genes to different stresses. In wheat seedlings and within 48 h of salt/drought stress or 4 days of nitrogen starvation stress, the autophagic activity of leaf tissues was activated by these three abiotic stresses and that of root tissues enhanced by drought and nitrogen starvation. This activated or enhanced autophagic activity was supported by up-regulated expression levels of ATG8s. Wheat ATG8s also responded to infection by the powdery mildew causal fungus, and their expression was inhibited in susceptible seedlings while repeatedly up-regulated in resistant seedlings during the early stage of pathogen infection. A comparison among the ATG8 family showed that different ATG8s had similar stress-regulated expression patterns and that several ATG8s were more sensitive to specific stresses. Collectively, these results suggest that the ATG8-requiring autophagy process is involved in wheat responses to stresses and that different ATG8s are commonly involved but have unequal significance in wheat response to specific stresses.
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References
Avin-Wittenberg T (2018) Autophagy and its role in plant abiotic stress management. Plant Cell Environ. https://doi.org/10.1111/pce.13404
Avin-Wittenberg T, Baluška F, Bozhkov PV, Elander PH, Fernie AR, Galili G, Hassan A, Hofius D, Isono E, Le Bars R, Masclaux-Daubresse C, Minina EA, Peled-Zehavi H, Coll NS, Sandalio LM, Satiat-Jeunemaitre B, Sirko A, Testillano PS, Batoko H (2018) Autophagy-related approaches for improving nutrient use efficiency and crop yield protection. J Exp Bot 69:1335–1353
Chen L, Liao B, Qi H, Xie LJ, Huang L, Tan WJ, Zhai N, Yuan LB, Zhou Y, Yu LJ, Chen QF, Shu W, Xiao S (2015) Autophagy contributes to regulation of the hypoxia response during submergence in Arabidopsis thaliana. Autophagy 11:2233–2246
Cheng F, Yin LL, Zhou J, Xia XJ, Shi K, Yu JQ, Zhou YH, Foyer CH (2016) Interactions between 2-Cys peroxiredoxins and ascorbate in autophagosome formation during the heat stress response in Solanum lycopersicum. J Exp Bot 67:1919–1933
Chung T, Suttangkakul A, Vierstra RD (2009) The ATG autophagic conjugation system in maize: ATG transcripts and abundance of the ATG8-lipid adduct are regulated by development and nutrient availability. Plant Physiol 49:220–234
Contento AL, Xiong Y, Bassham DC (2005) Visualization of autophagy in Arabidopsis using the fluorescent dye monodansylcadaverine and a GFP-AtATG8e fusion protein. Plant J 42:598–608
Hofius D, Li L, Hafrén A, Coll NS (2017) Autophagy as an emerging arena for plant-pathogen interactions. Curr Opin Plant Biol 38:117–123
Inoue Y, Suzuki T, Hattori M, Yoshimoto K, Ohsumi Y, Moriyasu Y (2006) AtATG genes, homologs of yeast autophagy genes, are involved in constitutive autophagy in Arabidopsis root tip cells. Plant Cell Physiol 47:1641–1652
Kabbage M, Williams B, Dickman MB (2013) Cell death control: the interplay of apoptosis and autophagy in the pathogenicity of Sclerotinia sclerotiorum. PLoS Pathog 9:e1003287
Kellner R, De la Concepcion JC, Maqbool A, Kamoun S, Dagdas YF (2017) ATG8 expansion: a driver of selective autophagy diversification? Trends Plant Sci 22:204–214
Ketelaar T, Voss C, Dimmock SA, Thumm M, Hussey PJ (2004) Arabidopsis homologues of the autophagy protein Atg8 are a novel family of microtubule binding proteins. FEBS Lett 567:302–306
Kuzuoglu-Ozturk D, Cebeci Yalcinkaya O, Akpinar BA, Mitou G, Korkmaz G, Gozuacik D, Budak H (2012) Autophagy-related gene, TdAtg8, in wild emmer wheat plays a role in drought and osmotic stress response. Planta 236:1081–1092
Lai Z, Wang F, Zheng Z, Fan B, Chen Z (2011) A critical role of autophagy in plant resistance to necrotrophic fungal pathogens. Plant J 66:953–968
Li F, Vierstra RD (2012) Autophagy: a multifaceted intracellular system for bulk and selective recycling. Trends Plant Sci 17:526–537
Li WW, Chen M, Zhong L, Liu JM, Xu ZS, Li LC, Zhou YB, Guo CH, Ma YZ (2015) Overexpression of the autophagy-related gene SiATG8a from foxtail millet (Setaria italica L.) confers tolerance to both nitrogen starvation and drought stress in Arabidopsis. Biochem Biophys Res Commun 468:800–806
Li W, Chen M, Wang E, Hu L, Hawkesford MJ, Zhong L, Chen Z, Xu Z, Li L, Zhou Y, Guo C, Ma Y (2016a) Genome-wide analysis of autophagy-associated genes in foxtail millet (Setaria italica L) and characterization of the function of SiATG8a in conferring tolerance to nitrogen starvation in rice. BMC Genomics 17:797
Li Y, Kabbage M, Liu W, Dickman MB (2016b) Aspartyl protease-mediated cleavage of BAG6 is necessary for autophagy and fungal resistance in plants. Plant Cell 28:233–247
Liu Y, Schiff M, Czymmek K, Tallo'czy Z, Levine B, Dinesh-Kumar SP (2005) Autophagy regulates programmed cell death during the plant innate immune response. Cell 121:567–577
Luo L, Zhang P, Zhu R, Fu J, Su J, Zheng J, Wang Z, Wang D, Gong Q (2017) Autophagy is rapidly induced by salt stress and is required for salt tolerance in Arabidopsis. Front Plant Sci 8:1459
Lytvyn DI, Olenieva VD, Yemets AI, Blume YB (2018) Histochemical analysis of tissue-specific α-tubulin acetylation as a response to autophagy induction by different stress factors in Arabidopsis thaliana. Cytol Genet 52:245–252
Mackeh R, Perdiz D, Lorin S, Codogno P, Poüs C (2013) Autophagy and microtubules—new story, old players. J Cell Sci 126:1071–1080
Michaeli S, Galili G, Genschik P, Fernie AR, Avin-Wittenberg T (2016) Autophagy in plants—what's new on the menu? Trends Plant Sci 21:134–144
Minina EA, Moschou PN, Vetukuri RR, Sanchez-Vera V, Cardoso C, Liu Q, Elander PH, Dalman K, Beganovic M, Lindberg Yilmaz J, Marmon S, Shabala L, Suarez MF, Ljung K, Novák O, Shabala S, Stymne S, Hofius D, Bozhkov PV (2018) Transcriptional stimulation of rate-limiting components of the autophagic pathway improves plant fitness. J Exp Bot 69:1415–1432
Nair U, Yen WL, Mari M, Cao Y, Xie Z, Baba M, Reggiori F, Klionsky DJ (2012) A role for Atg8-PE deconjugation in autophagosome biogenesis. Autophagy 8:780–793
Nakatogawa H, Ichimura Y, Ohsumi Y (2007) Atg8, a ubiquitin-like protein required for autophagosome formation, mediates membrane tethering and hemifusion. Cell 130:165–178
Olenieva V, Lytvyn D, Yemets A, Bergounioux C, Blume Y (2017) Tubulin acetylation accompanies autophagy development induced by different abiotic stimuli in Arabidopsis thaliana. Cell Biol Int. https://doi.org/10.1002/cbin.10843
Pei D, Zhang W, Sun H, Wei XJ, Yue JY, Wang HZ (2014) Identification of autophagy-related genes ATG4 and ATG8 from wheat (Triticum aestivum L.) and profiling of their expression patterns responding to biotic and abiotic stresses. Plant Cell Rep 33:1697–1710
Seo E, Woo J, Park E, Bertolani SJ, Siegel JB, Choi D, Dinesh-Kumar SP (2016) Comparative analyses of ubiquitin-like ATG8 and cysteine protease ATG4 autophagy. Autophagy 12:2054–2068
Thompson AR, Doelling JH, Suttangkakul A, Vierstra RD (2005) Autophagic nutrient recycling in Arabidopsis directed by the ATG8 and ATG12 conjugation pathways. Plant Physiol 138:2097–2110
Wang Y, Cai S, Yin L, Shi K, Xia X, Zhou Y, Yu J, Zhou J (2015) Tomato HsfA1a plays a critical role in plant drought tolerance by activating ATG genes and inducing autophagy. Autophagy 11:2033–2047
Wang P, Sun X, Jia X, Wang N, Gong X, Ma F (2016) Characterization of an autophagy-related gene MdATG8i from apple. Front Plant Sci 7:720
Wang P, Sun X, Wang N, Jia X, Ma F (2017a) Ectopic expression of an autophagy-associated MdATG7b gene from apple alters growth and tolerance to nutrient stress in Arabidopsis thaliana. Plant Cell Tiss Organ Cult 128:9–23
Wang P, Sun X, Jia X, Ma F (2017b) Apple autophagy-related protein MdATG3s afford tolerance to multiple abiotic stresses. Plant Sci 256:53–64
Wang FX, Luo YM, Ye ZQ, Cao X, Liang JN, Wang Q, Wu Y, Wu JH, Wang HY, Zhang M, Cheng HQ, Xia GX (2018) iTRAQ-based proteomics analysis of autophagy-mediated immune responses against the vascular fungal pathogen Verticillium dahliae in Arabidopsis. Autophagy 14:598–618
Xia T, Xiao D, Liu D, Chai W, Gong Q, Wang NN (2012) Heterologous expression of ATG8c from soybean confers tolerance to nitrogen deficiency and increases yield in Arabidopsis. PLoS ONE 7:e37217
Xie Z, Klionsky DJ (2007) Autophagosome formation: core machinery and adaptations. Nat Cell Biol 9:1102–1109
Xie Z, Nair U, Klionsky DJ (2008) Atg8 controls phagophore expansion during autophagosome formation. Mol Biol Cell 19:3290–3298
Yang Y, Guo Y (2018) Elucidating the molecular mechanisms mediating plant salt-stress responses. New Phytol 217:523–539
Yoshimoto K, Hanaoka H, Sato S, Kato T, Tabata S, Noda T, Ohsumi Y (2004) Processing of ATG8s, ubiquitin-like proteins, and their deconjugation by ATG4s are essential for plant autophagy. Plant Cell 16:2967–2983
Yue W, Nie X, Cui L, Zhi Y, Zhang T, Du X, Song W (2018) Genome-wide sequence and expressional analysis of autophagy gene family in bread wheat (Triticum aestivum L.). J Plant Physiol 229:7–21
Zhou XM, Zhao P, Wang W, Zou J, Cheng TH, Peng XB, Sun MX (2015) A comprehensive, genome-wide analysis of autophagy-related genes identified in tobacco suggests a central role of autophagy in plant response to various environmental cues. DNA Res 22:245–257
Funding
This work is supported by the Natural Science Foundation of Tianjin, China (17JCZDJC33800, 18JCYBJC30300); the Knowledge Innovation and Training Program of Tianjin, Tianjin Municipal Education Commission (135305JF78); and the Knowledge Innovation Program of Tianjin Normal University (1353P2XC1604, 135202RC1702).
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Zhang, J., Yang, W., Yue, J. et al. The Responses of Wheat Autophagy and ATG8 Family Genes to Biotic and Abiotic Stresses. J Plant Growth Regul 39, 867–876 (2020). https://doi.org/10.1007/s00344-019-10027-w
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DOI: https://doi.org/10.1007/s00344-019-10027-w