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Function and Transcriptional Regulation of Autophagy-related Genes in Plants

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  • Guangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Sciences, South China Normal University, Guangzhou 510631, China
First author contact:† These authors contributed equally to this paper

Received date: 2020-09-29

  Accepted date: 2020-12-25

  Online published: 2020-11-24

Abstract

Macroautophagy (hereafter termed autophagy) is an evolutionarily conserved cellular degradation and recyc- ling pathway in eukaryotes. In this pathway, cellular substances, such as dysfunctional proteins and damaged organelles, are sequestered by a double-membrane structure, autophagosome, and eventually delivered to the lysosomes or vacuoles for degradation and recycling. Autophagy plays essential roles in plant growth and development, as well as in response to environmental stresses. Up to now, more than 40 autophagy-related (ATG) genes have been identified in model plants such as Arabidopsis thaliana and Oryza sativa. It is well established that a large number of ATG genes are up-regulated during specific developmental stages such as leaf senescence and seed maturation, as well as when plants encounter adverse environmental conditions, for example, nutrient starvation, drought or pathogens infection and so on. However, the transcriptional activation or repression mechanisms of ATG genes during these biological processes are largely unknown and need further study. In this review, we summarized the roles and the well-established transcriptional regulation network of ATG genes during plant growth, development and stress responses.

Cite this article

Xibao Li, Minyi Lai, Shan Liang, Xiaojing Wang, Caiji Gao, Chao Yang . Function and Transcriptional Regulation of Autophagy-related Genes in Plants[J]. Chinese Bulletin of Botany, 2021 , 56(2) : 201 -217 . DOI: 10.11983/CBB20159

References

[1] 黄晓, 李发强 (2016). 细胞自噬在植物细胞程序性死亡中的作用. 植物学报 51,859-862.
[2] 刘洋, 张静, 王秋玲, 侯岁稳 (2018). 植物细胞自噬研究进展. 植物学报 53,5-16.
[3] 马丹颖, 季东超, 徐勇, 陈彤, 田世平 (2019). 活性氧调控植物细胞自噬的研究进展. 植物学报 54,81-92.
[4] 王燕, 刘玉乐 (2010). 植物细胞自噬研究进展. 中国细胞生物学学报 32,677-689.
[5] Avila-Ospina L, Moison M, Yoshimoto K, Masclaux-Daubresse C (2014). Autophagy, plant senescence, and nutrient recycling. J Exp Bot 65,3799-3811.
[6] Avin-Wittenberg T (2019). Autophagy and its role in plant abiotic stress management. Plant Cell Environ 42, 1045- 1053.
[7] Baumberger N, Tsai CH, Lie M, Havecker E, Baulcombe DC (2007). The polerovirus silencing suppressor P0 targets ARGONAUTE proteins for degradation. Curr Biol 17,1609-1614.
[8] Bewley JD (1997). Seed germination and dormancy. Plant Cell 9,1055-1066.
[9] Blümel M, Dally N, Jung C (2015). Flowering time regula- tion in crops—what did we learn fromArabidopsis? Curr Opin Biotechnol 32,121-129.
[10] Breeze E, Harrison E, McHattie S, Hughes L, Hickman R, Hill C, Kiddle S, Kim YS, Penfold CA, Jenkins D, Zhang C, Morris K, Jenner C, Jackson S, Thomas B, Tabrett A, Legaie R, Moore JD, Wild DL, Ott S, Rand D, Beynon J, Denby K, Mead A, Buchanan-Wollaston V (2011). High-resolution temporal profiling of transcripts during Arabidopsis leaf senescence reveals a distinct chronology of processes and regulation. Plant Cell 23,873-894.
[11] Buchanan-Wollaston V, Page T, Harrison E, Breeze E, Lim PO, Nam HG, Lin JF, Wu SH, Swidzinski J, Ishizaki K, Leaver CJ (2005). Comparative transcriptome analysis reveals significant differences in gene expression and signaling pathways between developmental and dark/ starvation-induced senescence in Arabidopsis. Plant J 42,567-585.
[12] Chen L, Liao B, Qi H, Xie LJ, Huang L, Tan WJ, Zhai N, Yuan LB, Zhou Y, Yu LJ, Chen QF, Shu WS, Xiao S (2015). Autophagy contributes to regulation of the hypoxia response during submergence in Arabidopsis thaliana. Autophagy 11,2233-2246.
[13] Chi C, Li XM, Fang PP, Xia XJ, Shi K, Zhou YH, Zhou J, Yu JQ (2020). Brassinosteroids act as a positive regulator of NBR1-dependent selective autophagy in response to chilling stress in tomato. J Exp Bot 71,1092-1106.
[14] Derrien B, Baumberger N, Schepetilnikov M, Viotti C, De Cillia J, Ziegler-Graff V, Isono E, Schumacher K, Genschik P (2012). Degradation of the antiviral compo- nent ARGONAUTE1 by the autophagy pathway. Proc Natl Acad Sci USA 109,15942-15946.
[15] Deter RL, Baudhuin P, De Duve C (1967). Participation of lysosomes in cellular autophagy induced in rat liver by glucagon. J Cell Biol 35,C11-C16.
[16] Di Bartolomeo S, Nazio F, Cecconi F (2010). The role of autophagy during development in higher eukaryotes. Traffic 11,1280-1289.
[17] Di Berardino J, Marmagne A, Berger A, Yoshimoto K, Cueff G, Chardon F, Masclaux-Daubresse C, Reisdorf- Cren M (2018). Autophagy controls resource allocation and protein storage accumulation in Arabidopsis seeds. J Exp Bot 69,1403-1414.
[18] Doelling JH, Walker JM, Friedman EM, Thompson AR, Vierstra RD (2002). The APG8/12-activating enzyme APG7 is required for proper nutrient recycling and sene- scence in Arabidopsis thaliana. J Biol Chem 277, 33105- 33114.
[19] Dündar G, Shao ZH, Higashitani N, Kikuta M, Izumi M, Higashitani A (2019). Autophagy mitigates high-tem- perature injury in pollen development of Arabidopsis thaliana. Dev Biol 456,190-200.
[20] Eguchi M, Kimura K, Makino A, Ishida H (2017). Autophagy is induced under Zn limitation and contributes to Zn-limited stress tolerance in Arabidopsis (Arabidopsis thaliana). Soil Sci Plant Nutr 63,342-350.
[21] Fan T, Yang W, Zeng X, Xu XL, Xu YL, Fan XR, Luo M, Tian CG, Xia KF, Zhang MY (2020). A rice autophagy gene OsATG8b is involved in nitrogen remobilization and control of grain quality. Front Plant Sci 11,588.
[22] Fujiki Y, Yoshimoto K, Ohsumi Y (2007). An Arabidopsis homolog of yeast ATG6/ VPS30 is essential for pollen germination. Plant Physiol 143,1132-1139.
[23] Gallegos J (2018). Autophagy: both friend and foe in Pseudomonas syringae infection. Plant Cell 30,522-523.
[24] Gangappa SN, Botto JF (2016). The multifaceted roles of HY5 in plant growth and development. Mol Plant 9, 1353-1365.
[25] Gao CJ, Zhuang XH, Shen JB, Jiang LW (2017). Plant ESCRT complexes: moving beyond endosomal sorting. Trends Plant Sci 22,986-998.
[26] Garapati P, Feil R, Lunn JE, Van Dijck P, Balazadeh S, Mueller-Roeber B (2015). Transcription factor Arabidop- sis activating factor 1 integrates carbon starvation res- ponses with trehalose metabolism. Plant Physiol 169,379-390.
[27] Goring DR (2017). Exocyst, exosomes, and autophagy in the regulation of Brassicaceae pollen-stigma interactions. J Exp Bot 69,69-78.
[28] Gou WT, Li X, Guo SY, Liu YF, Li FQ, Xie QJ (2019). Autophagy in plant: a new orchestrator in the regulation of the phytohormones homeostasis. Int J Mol Sci 20,2900.
[29] Guiboileau A, Yoshimoto K, Soulay F, Bataillé MP, Avice JC, Masclaux-Daubresse C (2012). Autophagy machi- nery controls nitrogen remobilization at the whole-plant level under both limiting and ample nitrate conditions in Arabidopsis. New Phytol 194,732-740.
[30] Hafrén A, Macia JL, Love AJ, Milner JJ, Drucker M, Hofius D (2017). Selective autophagy limits cauliflower mosaic virus infection by NBR1-mediated targeting of viral capsid protein and particles. Proc Natl Acad Sci USA 114,E2026-E2035.
[31] Hafrén A, Ustün S, Hochmuth A, Svenning S, Johansen T, Hofius D (2018). Turnip Mosaic virus counteracts selective autophagy of the viral silencing suppressor HCpro. Plant Physiol 176,649-662.
[32] Han B, Xu H, Feng YT, Xu W, Cui QH, Liu AZ (2020). Genomic characterization and expressional profiles of autophagy-related genes ( ATGs) in oilseed crop castor bean ( Ricinus communis L.). Int J Mol Sci 21,562.
[33] Hanaoka H, Noda T, Shirano Y, Kato T, Hayashi H, Shibata D, Tabata S, Ohsumi Y (2002). Leaf sene- scence and starvation-induced chlorosis are accelerated by the disruption of an Arabidopsis autophagy gene. Plant Physiol 129,1181-1193.
[34] Harrison-Lowe NJ, Olsen LJ (2008). Autophagy protein 6 (ATG6) is required for pollen germination in Arabidopsis thaliana. Autophagy 4,339-348.
[35] Haxim Y, Ismayil A, Jia Q, Wang Y, Zheng XY, Chen TY, Qian LC, Liu N, Wang YJ, Han SJ, Cheng JX, Qi YJ, Hong YG, Liu YL (2017). Autophagy functions as an antiviral mechanism against geminiviruses in plants. eLife 6,e23897.
[36] Hightower LE (1991). Heat shock, stress proteins, chapero- nes, and proteotoxicity. Cell 66,191-197.
[37] Huang X, Zheng C, Liu F, Yang C, Zheng P, Lu X, Tian J, Chung T, Otegui MS, Xiao S, Gao C, Vierstra RD, Li F (2019). Genetic analyses of the Arabidopsis ATG1 kinase complex reveal both kinase-dependent and independent autophagic routes during fixed-carbon starvation. Plant Cell 31,2973-2995.
[38] Jakoby M, Weisshaar B, Dr?ge-Laser W, Vicente-Car- bajosa J, Tiedemann J, Kroj T, Parcy F (2002). bZIP transcription factors in Arabidopsis. Trends Plant Sci 7,106-111.
[39] Jiao YL, Lau OS, Deng XW (2007). Light-regulated trans- criptional networks in higher plants. Nat Rev Genet 8,217-230.
[40] Jung H, Lee HN, Marshall RS, Lomax AW, Yoon MJ, Kim J, Kim JH, Vierstra RD, Chung T (2020). Arabidopsis cargo receptor NBR1 mediates selective autophagy of defective proteins. J Exp Bot 71,73-89.
[41] Kurusu T, Koyano T, Hanamata S, Kubo T, Noguchi Y, Yagi C, Nagata N, Yamamoto T, Ohnishi T, Okazaki Y, Kitahata N, Ando D, Ishikawa M, Wada S, Miyao A, Hirochika H, Shimada H, Makino A, Saito K, Ishida H, Kinoshita T, Kurata N, Kuchitsu K (2014). OsATG7 is required for autophagy-dependent lipid metabolism in rice postmeiotic anther development. Autophagy 10,878-888.
[42] Lai ZB, Wang F, Zheng ZY, Fan BF, Chen ZX (2011). A critical role of autophagy in plant resistance to necro- trophic fungal pathogens. Plant J 66,953-968.
[43] Leary AY, Sanguankiattichai N, Duggan C, Tumtas Y, Pandey P, Segretin ME, Linares JS, Savage ZD, Yow RJ, Bozkurt TO (2018). Modulation of plant autophagy during pathogen attack. J Exp Bot 69,1325-1333.
[44] Leng X, Jia HF, Sun X, Shangguan LF, Mu Q, Wang BJ, Fang JG (2015). Comparative transcriptome analysis of grapevine in response to copper stress. Sci Rep 5,17749.
[45] Li FF, Zhang CW, Li YZ, Wu GW, Hou XL, Zhou XP, Wang AM (2018). Beclin1 restricts RNA virus infection in plants through suppression and degradation of the viral poly- merase. Nat Commun 9,1268.
[46] Li FQ, Chung T, Pennington JG, Federico ML, Kaeppler HF, Kaeppler SM, Otegui MS, Vierstra RD (2015). Autophagic recycling plays a central role in maize nitro- gen remobilization. Plant Cell 27,1389-1408.
[47] Li FQ, Chung T, Vierstra RD (2014). AUTOPHAGY-RE- LATED11 plays a critical role in general autophagy- and senescence-induced mitophagy in Arabidopsis. Plant Cell 26,788-807.
[48] Li FQ, Vierstra RD (2012). Autophagy: a multifaceted intracellular system for bulk and selective recycling. Trends Plant Sci 17,526-537.
[49] Li SS, Yan H, Mei WM, Tse YC, Wang H (2020). Boosting autophagy in sexual reproduction: a plant perspective. New Phytol 226,679-689.
[50] Liao CY, Bassham DC (2020). Combating stress: the interplay between hormone signaling and autophagy in plants. J Exp Bot 71,1723-1733.
[51] Lindemose S, Jensen MK, Van De Velde J, O'Shea C, Heyndrickx KS, Workman CT, Vandepoele K, Skriver K, De Masi F (2014). A DNA-binding-site landscape and regulatory network analysis for NAC transcription factors in Arabidopsis thaliana. Nucleic Acids Res 42, 7681- 7693.
[52] Liu F, Hu WM, Vierstra RD (2018). The vacuolar protein sorting-38 subunit of the Arabidopsis phosphatidylinositol- 3-kinase complex plays critical roles in autophagy, endosome sorting, and gravitropism. Front Plant Sci 9,781.
[53] Liu GY, Zeng HQ, Li X, Wei YX, Shi HT (2019). Functional analysis of MaWRKY24 in transcriptional activation of autophagy-related gene 8f/ g and plant disease suscep- tibility to soil-borne Fusarium oxysporum f. sp. cubense. Pathogens 8,264.
[54] Liu YL, Schiff M, Czymmek K, Tallóczy Z, Levine B, Dinesh-Kumar SP (2005). Autophagy regulates program- med cell death during the plant innate immune response. Cell 121,567-577.
[55] Liu YM, Xiong Y, Bassham DC (2009). Autophagy is required for tolerance of drought and salt stress in plants. Autophagy 5,954-963.
[56] Luo LM, Zhang PP, Zhu RH, Fu J, Su J, Zheng J, Wang ZY, Wang D, Gong QQ (2017). Autophagy is rapidly induced by salt stress and is required for salt tolerance in Arabidopsis. Front Plant Sci 8, 1459.
[57] Maleck K, Levine A, Eulgem T, Morgan A, Schmid J, Lawton KA, Dangl JL, Dietrich RA (2000). The trans- criptome of Arabidopsis thaliana during systemic acquired resistance. Nat Genet 26,403-410.
[58] Marshall RS, Vierstra RD (2018). Autophagy: the master of bulk and selective recycling. Annu Rev Plant Biol 69,173- 208.
[59] Masclaux-Daubresse C, Chen QW, Have M (2017). Regu- lation of nutrient recycling via autophagy. Curr Opin Plant Biol 39,8-17.
[60] Michaeli S, Clavel M, Lechner E, Viotti C, Wu J, Dubois M, Hacquard T, Derrien B, Izquierdo E, Lecorbeiller M, Bouteiller N, De Cilia J, Ziegler-Graff V, Vaucheret H, Galili G, Genschik P (2019). The viral F-box protein P0 induces an ER-derived autophagy degradation pathway for the clearance of membrane-bound AGO1. Proc Natl Acad Sci USA 116,22872-22883.
[61] Minina EA, Moschou PN, Vetukuri RR, Sanchez-Vera V, Cardoso C, Liu QS, Elander PH, Dalman K, Beganovic M, Yilmaz JL, Marmon S, Shabala L, Suarez MF, Ljung K, Novák O, Shabala S, Stymne S, Hofius D, Bozhkov PV (2018). Transcriptional stimulation of rate-limiting com- ponents of the autophagic pathway improves plant fitness. J Exp Bot 69,1415-1432.
[62] Naumann C, Müller J, Sakhonwasee S, Wieghaus A, Hause G, Heisters M, Bürstenbinder K, Abel S (2019). The local phosphate deficiency response activates endo- plasmic reticulum stress-dependent autophagy. Plant Phy- siol 179,460-476.
[63] Osterlund MT, Hardtke CS, Wei N, Deng XW (2000). Targeted destabilization of HY5 during light-regulated development of Arabidopsis. Nature 405,462-466.
[64] Pu YT, Luo XJ, Bassham DC (2017). TOR-dependent and -independent pathways regulate autophagy in Arabi- dopsis thaliana. Front Plant Sci 8, 1204.
[65] Qin GJ, Ma ZQ, Zhang L, Xing SF, Hou XH, Deng J, Liu JJ, Chen ZL, Qu LJ, Gu HY (2007). Arabidopsis AtBECLIN1/ AtAtg6/ AtVps30 is essential for pollen germi- nation and plant development. Cell Res 17,249-263.
[66] Ren CX, Liu JF, Gong QQ (2014). Functions of autophagy in plant carbon and nitrogen metabolism. Front Plant Sci 5,301.
[67] Rodrigues J, Inzé D, Nelissen H, Saibo NJM (2019). Source-sink regulation in crops under water deficit. Trends Plant Sci 24,652-663.
[68] Rodriguez E, Chevalier J, Olsen J, Ansb?l J, Kapousidou V, Zuo ZL, Svenning S, Loefke C, Koemeda S, Drozdowskyj PS, Jez J, Durnberger G, Kuenzl F, Schutzbier M, Mechtler K, Ebstrup EN, Lolle S, Dagdas Y, Petersen M (2020). Autophagy mediates temporary reprogramming and dedifferentiation in plant somatic cells. EMBO J 39,e103315.
[69] Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010). WRKY transcription factors. Trends Plant Sci 15,247-258.
[70] Sedaghatmehr M, Thirumalaikumar VP, Kamranfar I, Marmagne A, Masclaux-Daubresse C, Balazadeh S (2019). A regulatory role of autophagy for resetting the memory of heat stress in plants. Plant Cell Environ 42,1054-1064.
[71] Shangguan LF, Fang X, Chen LD, Cui LW, Fang JG (2018). Genome-wide analysis of autophagy-related ge- nes (ARGs) in grapevine and plant tolerance to copper stress. Planta 247,1449-1463.
[72] Shibuya K, Niki T, Ichimura K (2013). Pollination induces autophagy in petunia petals via ethylene. J Exp Bot 64,1111-1120.
[73] Signorelli S, Tarkowski ?P, Van Den Ende W, Bassham DC (2019). Linking autophagy to abiotic and biotic stress responses. Trends Plant Sci 24,413-430.
[74] Suzuki N, Rivero RM, Shulaev V, Blumwald E, Mittler R (2014). Abiotic and biotic stress combinations. New Phytol 203,32-43.
[75] Takahashi S, Murata N (2008). How do environmental stresses accelerate photoinhibition? Trends Plant Sci 13,178-182.
[76] Takeshige K, Baba M, Tsuboi S, Noda T, Ohsumi Y (1992). Autophagy in yeast demonstrated with proteinase- deficient mutants and conditions for its induction. J Cell Biol 119,301-311.
[77] Tasaki M, Asatsuma S, Matsuoka K (2014). Monitoring protein turnover during phosphate starvation-dependent autophagic degradation using a photoconvertible fluores- cent protein aggregate in tobacco BY-2 cells. Front Plant Sci 5,172.
[78] Tsukada M, Ohsumi Y (1993). Isolation and characteri- zation of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett 333,169-174.
[79] Ustün S, Hafrén A, Liu QS, Marshall RS, Minina EA, Bozhkov PV, Vierstra RD, Hofius D (2018). Bacteria exploit autophagy for proteasome degradation and en- hanced virulence in plants. Plant Cell 30,668-685.
[80] Van Der Graaff E, Schwacke R, Schneider A, Desimone M, Flügge UI, Kunze R (2006). Transcription analysis of Arabidopsis membrane transporters and hormone path- ways during developmental and induced leaf senescence. Plant Physiol 141,776-792.
[81] Von Koskull-Doring P, Scharf KD, Nover L (2007). The diversity of plant heat stress transcription factors. Trends Plant Sci 12,452-457.
[82] Wada S, Hayashida Y, Izumi M, Kurusu T, Hanamata S, Kanno K, Kojima S, Yamaya T, Kuchitsu K, Makino A, Ishida H (2015). Autophagy supports biomass production and nitrogen use efficiency at the vegetative stage in rice. Plant Physiol 168,60-73.
[83] Wang P, Nolan TM, Yin YH, Bassham DC (2020). Identi- fication of transcription factors that regulate ATG8 expres- sion and autophagy in Arabidopsis. Autophagy 16, 123- 139.
[84] Wang P, Sun X, Wang N, Jia X, Ma FW (2017). Ectopic expression of an autophagy-associated MdATG7b gene from apple alters growth and tolerance to nutrient stress in Arabidopsis thaliana. Plant Cell Tissue Organ Cult 128,9-23.
[85] Wang Y, Cai SY, Yin LL, Shi K, Xia XJ, Zhou YH, Yu JQ, Zhou J (2015). Tomato HsfA1a plays a critical role in plant drought tolerance by activating ATG genes and inducing autophagy. Autophagy 11,2033-2047.
[86] Wang Y, Cao JJ, Wang KX, Xia XJ, Shi K, Zhou YH, Yu JQ, Zhou J (2019). BZR1 mediates brassinosteroid- induced autophagy and nitrogen starvation in tomato. Plant Physiol 179,671-685.
[87] Wang Y, Yu BJ, Zhao JP, Guo JB, Li Y, Han SJ, Huang L, Du YM, Hong YG, Tang D, Liu YL (2013). Autophagy contributes to leaf starch degradation. Plant Cell 25, 1383- 1399.
[88] Wei YX, Liu W, Hu W, Liu GY, Wu CJ, Liu W, Zeng HQ, He CZ, Shi HT (2017). Genome-wide analysis of autophagy- related genes in banana highlights MaATG8s in cell death and autophagy in immune response to Fusarium wilt. Plant Cell Rep 36,1237-1250.
[89] Williams B, Njaci I, Moghaddam L, Long H, Dickman MB, Zhang XR, Mundree S (2015). Trehalose accumulation triggers autophagy during plant desiccation. PLoS Genet 11,e1005705.
[90] Woo HR, Kim HJ, Lim PO, Nam HG (2019). Leaf senes- cence: systems and dynamics aspects. Annu Rev Plant Biol 70,347-376.
[91] Wu YR, Deng ZY, Lai JB, Zhang YY, Yang CP, Yin BJ, Zhao QZ, Zhang L, Li Y, Yang CW, Xie Q (2009). Dual function of Arabidopsis ATAF1 in abiotic and biotic stress responses. Cell Res 19,1279-1290.
[92] Xia KF, Liu T, Ouyang J, Wang R, Fan T, Zhang MY (2011). Genome-wide identification, classification, and expression analysis of autophagy-associated gene homo- logues in rice ( Oryza sativa L.). DNA Res 18,363-377.
[93] Xia XJ, Fang PP, Guo X, Qian XJ, Zhou J, Shi K, Zhou YH, Yu JQ (2018). Brassinosteroid-mediated apoplastic H 2O 2-glutaredoxin 12/14 cascade regulates antioxidant capacity in response to chilling in tomato. Plant Cell En- viron 41,1052-1064.
[94] Xiong Y, Contento AL, Nguyen PQ, Bassham DC (2007). Degradation of oxidized proteins by autophagy during oxidative stress in Arabidopsis. Plant Physiol 143, 291- 299.
[95] Yamauchi S, Mano S, Oikawa K, Hikino K, Teshima KM, Kimori Y, Nishimura M, Shimazaki KI, Takemiya A (2019). Autophagy controls reactive oxygen species homeostasis in guard cells that is essential for stomatal opening. Proc Natl Acad Sci USA 116,19187-19192.
[96] Yan HY, Liu Y, Zhang K, Song J, Xu WY, Su Z (2019). Chromatin state-based analysis of epigenetic H3K4me3 marks of Arabidopsis in response to dark stress. Front Genet 10,306.
[97] Yan Y, Wang P, He CZ, Shi HT (2017). MeWRKY20 and its interacting and activating autophagy-related protein 8 (MeATG8) regulate plant disease resistance in cassava. Biochem Biophys Res Commun 494,20-26.
[98] Yang C, Shen WJ, Yang LM, Sun Y, Li XB, Lai MY, Wei J, Wang CJ, Xu YC, Li FQ, Liang S, Yang CW, Zhong SW, Luo M, Gao CJ (2020a). HY5-HDA9 module transcrip- tionally regulates plant autophagy in response to light-to- dark conversion and nitrogen starvation. Mol Plant 13,515-531.
[99] Yang M, Ismayil A, Liu YL (2020b). Autophagy in plant- virus interactions. Annu Rev Virol 7,403-419.
[100] Ye H, Ren F, Guo HY, Guo LP, Bai JF, Wang YK (2020). Identification of key genes and transcription factors in ageing Arabidopsis papilla cells by transcriptome analy- sis. Plant Phys Biochem 147,1-9.
[101] Yoshida T, Ohama N, Nakajima J, Kidokoro S, Mizoi J, Nakashima K, Maruyama K, Kim JM, Seki M, Todaka D, Osakabe Y, Sakuma Y, Sch?ffl F, Shinozaki K, Yamaguchi-Shinozaki K (2011). Arabidopsis HsfA1 transcription factors function as the main positive regu- lators in heat shock-responsive gene expression. Mol Genet Genom 286,321-332.
[102] Yu JL, Zhen XX, Li X, Li N, Xu F (2019). Increased auto- phagy of rice can increase yield and nitrogen use ef- ficiency (NUE). Front Plant Sci 10,584.
[103] Yue WJ, Nie XJ, Cui LC, Zhi YQ, Zhang T, Du XL, Song WN (2018). Genome-wide sequence and expressional analysis of autophagy gene family in bread wheat ( Tri- ticum aestivum L.). J Plant Physiol 229,7-21.
[104] Zhai YF, Guo M, Wang H, Lu JP, Liu JH, Zhang C, Gong ZH, Lu MH (2016). Autophagy, a conserved mechanism for protein degradation, responds to heat, and other abiotic stresses in Capsicum annuum L. Front Plant Sci 7,131.
[105] Zhang JZ, Yang WW, Yue JY, Liu YN, Pei D, Wang HZ (2020). The responses of wheat autophagy and ATG8 family genes to biotic and abiotic stresses. J Plant Growth Regul 39,867-876.
[106] Zhang Y, Li S, Zhou LZ, Fox E, Pao J, Sun W, Zhou C, McCormick S (2011). Overexpression of Arabidopsis thaliana PTEN caused accumulation of autophagic bodies in pollen tubes by disrupting phosphatidylinositol 3-phos- phate dynamics. Plant J 68,1081-1092.
[107] Zhao P, Zhou XM, Zhao LL, Cheung AY, Sun MX (2020). Autophagy-mediated compartmental cytoplasmic deletion is essential for tobacco pollen germination and male fertility. Autophagy 16,2180-2192.
[108] Zhen XX, Xu F, Zhang WZ, Li N, Li X (2019). Overex- pression of rice gene OsATG8b confers tolerance to nitrogen starvation and increases yield and nitrogen use efficiency (NUE) in Arabidopsis. PLoS One 14, e0223011.
[109] Zhou J, Wang J, Yu JQ, Chen ZX (2014). Role and regulation of autophagy in heat stress responses of to- mato plants. Front Plant Sci 5,174.
[110] 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.
[111] Zhu T, Zou LJ, Li Y, Yao XH, Xu F, Deng XG, Zhang DW, Lin HH (2018). Mitochondrial alternative oxidase-depen- dent autophagy involved in ethylene-mediated drought tolerance in Solanum lycopersicum. Plant Biotechnol J 16, 2063-2076.
[112] Zhuang XH, Wang H, Lam SK, Gao CJ, Wang XF, Cai Y, Jiang LW (2013). A BAR-domain protein SH3P2, which binds to phosphatidylinositol 3-phosphate and ATG8, regulates autophagosome formation in Arabidopsis. Plant Cell 25,4596-4615.
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