Autophagy-related protein PlATG2 regulates the vegetative growth, sporangial cleavage, autophagosome formation, and pathogenicity of peronophythora litchii

References

• Kamoun S. Molecular genetics of pathogenic oomycetes. Eukaryot Cell. 2003;2(2):191–13. doi: 10.1128/EC.2.2.191-199.2003
   PubMedGoogle Scholar
• Kamoun S, Furzer O, Jones JD, et al. The top 10 oomycete pathogens in molecular plant pathology. Molecular Plant Pathology. 2015;16(4):413–434. doi: 10.1111/mpp.12190
   PubMed Web of Science ®Google Scholar
• Kao CW, Leu LS. Sporangium germination of peronophythora litchii, the causal organism of litchi downy blight. Mycologia. 1980;72(4):737–748. doi: 10.1080/00275514.1980.12021242
   Web of Science ®Google Scholar
• Wang HC, Sun HY, Stammler G, et al. Baseline and differential sensitivity of peronophythora litchii (lychee downy blight) to three carboxylic acid amide fungicides. Plant Pathology. 2009;58(3):571–576. doi: 10.1111/j.1365-3059.2008.01990.x
   Web of Science ®Google Scholar
• Xu L, Xue J, Wu P, et al. Antifungal activity of hypothemycin against peronophythora litchii in vitro and in vivo. J Agric Food Chem. 2013;61(42):10091–10095. doi: 10.1021/jf4030882
   PubMed Web of Science ®Google Scholar
• Carlsson SR, Simonsen A. Membrane dynamics in autophagosome biogenesis. J Cell Sci. 2015;128:193–205. doi: 10.1242/jcs.141036
   PubMed Web of Science ®Google Scholar
• Huang WP, Klionsky DJ. Autophagy in yeast: a review of the molecular machinery. Cell Struct Funct. 2002;27(6):409–420. doi: 10.1247/csf.27.409
   PubMed Web of Science ®Google Scholar
• Fukuda T, Furukawa K, Maruyama T, et al. Mitofissin: a novel mitochondrial fission protein that facilitates mitophagy. Autophagy. 2023a;19(11):1–3. doi: 10.1080/15548627.2023.2237343
   PubMed Web of Science ®Google Scholar
• Fukuda T, Furukawa K, Maruyama T, et al. The mitochondrial intermembrane space protein mitofissin drives mitochondrial fission required for mitophagy. Mol Cell. 2023b;83(12):2045–2058 e2049. doi: 10.1016/j.molcel.2023.04.022
   PubMed Web of Science ®Google Scholar
• Fukuda T, Kanki T. Atg43, a novel autophagy-related protein, serves as a mitophagy receptor to bridge mitochondria with phagophores in fission yeast. Autophagy. 2021;17(3):826–827. doi: 10.1080/15548627.2021.1874662
   PubMed Web of Science ®Google Scholar
• Suzuki K, Ohsumi Y. Current knowledge of the pre-autophagosomal structure (PAS). FEBS Lett. 2010;584(7):1280–1286. doi: 10.1016/j.febslet.2010.02.001
   PubMed Web of Science ®Google Scholar
• Jiang Z, Zhu L, Wang Q, et al. Autophagy-related 2 regulates chlorophyll degradation under abiotic stress conditions in Arabidopsis. Int J Mol Sci. 2020;21(12):4515. doi: 10.3390/ijms21124515
   PubMed Web of Science ®Google Scholar
• Obara K, Sekito T, Niimi K, et al. The Atg18-Atg2 complex is recruited to autophagic membranes via phosphatidylinositol 3-phosphate and exerts an essential function. J Biol Chem. 2008;283(35):23972–23980. doi: 10.1074/jbc.M803180200
   PubMed Web of Science ®Google Scholar
• Suzuki K, Kubota Y, Sekito T, et al. Hierarchy of Atg proteins in pre-autophagosomal structure organization. Genes Cells. 2007;12(2):209–218. doi: 10.1111/j.1365-2443.2007.01050.x
   PubMed Web of Science ®Google Scholar
• Kotani T, Kirisako H, Koizumi M, et al. The Atg2-Atg18 complex tethers pre-autophagosomal membranes to the endoplasmic reticulum for autophagosome formation. Proc Natl Acad Sci USA. 2018;115(41):10363–10368. doi: 10.1073/pnas.1806727115
   PubMed Web of Science ®Google Scholar
• Feng Y, He D, Yao Z, et al. The machinery of macroautophagy. Cell Res. 2014;24(1):24–41. doi: 10.1038/cr.2013.168
   PubMed Web of Science ®Google Scholar
• Gomez-Sanchez R, Rose J, Guimaraes R, et al. Atg9 establishes Atg2-dependent contact sites between the endoplasmic reticulum and phagophores. J Cell Bio. 2018;217(8):2743–2763. doi: 10.1083/jcb.201710116
   PubMed Web of Science ®Google Scholar
• Tang Z, Takahashi Y, He H, et al. TOM40 targets Atg2 to mitochondria-associated ER membranes for phagophore expansion. Cell Rep. 2019;28(7):1744–1757 e1745. doi: 10.1016/j.celrep.2019.07.036
   PubMed Web of Science ®Google Scholar
• Kang S, Shin KD, Kim JH, et al. Autophagy-related (ATG) 11, ATG9 and the phosphatidylinositol 3-kinase control ATG2-mediated formation of autophagosomes in arabidopsis. Plant Cell Rep. 2018;37(4):653–664. doi: 10.1007/s00299-018-2258-9
   PubMed Web of Science ®Google Scholar
• Luo M, Law KC, He Y, et al. Arabidopsis autophagy-related 2 is essential for ATG18a and ATG9 trafficking during autophagosome closure. Plant Physiol kiad. 2023;287(1):304–321. doi: 10.1093/plphys/kiad287
   Google Scholar
• Mishra D. Closing the loop: three musketeers of autophagy-ATG2, ATG18a, and ATG9. Plant Physiol kiad. 2023;369(1):177–178. doi: 10.1093/plphys/kiad369
   Google Scholar
• Asakura M, Ninomiya S, Sugimoto M, et al. Atg26-mediated pexophagy is required for host invasion by the plant pathogenic fungus Colletotrichum orbiculare. Plant Cell. 2009;21(4):1291–1304. doi: 10.1105/tpc.108.060996
   PubMed Web of Science ®Google Scholar
• Kershaw MJ, Talbot NJ. Genome-wide functional analysis reveals that infection-associated fungal autophagy is necessary for rice blast disease. Proc Natl Acad Sci U S A. 2009;106(37):15967–15972. doi: 10.1073/pnas.0901477106
   PubMed Web of Science ®Google Scholar
• Kikuma T, Ohneda M, Arioka M, et al. Functional analysis of the ATG8 homologue Aoatg8 and role of autophagy in differentiation and germination in aspergillus oryzae. Eukaryot Cell. 2006;5(8):1328–1336. doi: 10.1128/EC.00024-06
   PubMedGoogle Scholar
• Lv W, Wang C, Yang N, et al. Genome-wide functional analysis reveals that autophagy is necessary for growth, sporulation, deoxynivalenol production and virulence in fusarium graminearum. Sci Rep. 2017;7(1):11062. doi: 10.1038/s41598-017-11640-z
   PubMedGoogle Scholar
• Voigt O, Poggeler S. Autophagy genes Smatg8 and Smatg4 are required for fruiting-body development, vegetative growth and ascospore germination in the filamentous ascomycete sordaria macrospora. Autophagy. 2013;9(1):33–49. doi: 10.4161/auto.22398
   PubMed Web of Science ®Google Scholar
• Yue JY, Wang YJ, Jiao JL, et al. Silencing of ATG2 and ATG7 promotes programmed cell death in wheat via inhibition of autophagy under salt stress. Ecotoxicol Environ Saf. 2021;225:112761. doi: 10.1016/j.ecoenv.2021.112761
   PubMed Web of Science ®Google Scholar
• Zhao X, Feng W, Zhu X, et al. Conserved autophagy pathway contributes to stress tolerance and virulence and differentially controls autophagic flux upon nutrient starvation in Cryptococcus neoformans. Front Microbiol. 2019;10:2690. doi: 10.3389/fmicb.2019.02690
   PubMed Web of Science ®Google Scholar
• Yamauchi S, Mano S, Oikawa K, et al. Autophagy controls reactive oxygen species homeostasis in guard cells that is essential for stomatal opening. Proc Natl Acad Sci U S A. 2019;116(38):19187–19192. doi: 10.1073/pnas.1910886116
   PubMed Web of Science ®Google Scholar
• Yoshimoto K, Jikumaru Y, Kamiya Y, et al. Autophagy negatively regulates cell death by controlling NPR1-dependent salicylic acid signaling during senescence and the innate immune response in Arabidopsis. Plant Cell. 2009;21(9):2914–2927. doi: 10.1105/tpc.109.068635
   PubMed Web of Science ®Google Scholar
• Wang Y, Nishimura MT, Zhao T, et al. ATG2, an autophagy-related protein, negatively affects powdery mildew resistance and mildew-induced cell death in Arabidopsis. Plant J. 2011a;68(1):74–87. doi: 10.1111/j.1365-313X.2011.04669.x
   PubMed Web of Science ®Google Scholar
• Wang Y, Wu Y, Tang D. The autophagy gene, ATG18a, plays a negative role in powdery mildew resistance and mildew-induced cell death in Arabidopsis. Plant Signal Behav. 2011b;6(9):1408–1410. doi: 10.4161/psb.6.9.16967
   PubMedGoogle Scholar
• Hashimi SM, Wu NN, Ran J, et al. Silencing autophagy-related gene 2 (ATG2) results in accelerated senescence and enhanced immunity in soybean. Int J Mol Sci. 2021;22(21):11749. doi: 10.3390/ijms222111749
   PubMed Web of Science ®Google Scholar
• Chen L, Zhang X, Wang W, et al. Network and role analysis of autophagy in Phytophthora sojae. Sci Rep. 2017;7(1):1879. doi: 10.1038/s41598-017-01988-7
   PubMed Web of Science ®Google Scholar
• Luo Q, Wang FX, Zhong NQ, et al. The role of autophagy during development of the oomycete pathogen phytophthora infestans. J Genet Genomics. 2014;41(4):225–228. doi: 10.1016/j.jgg.2014.03.004
   PubMed Web of Science ®Google Scholar
• Wang J, Zhou G, Huang W, et al. Autophagy-related gene PlAtg6a is involved in mycelial growth, asexual reproduction and tolerance to salt and oxidative stresses in Peronophythora litchii. Int J Mol Sci. 2022;23(3):1839. doi: 10.3390/ijms23031839
   PubMed Web of Science ®Google Scholar
• Qiu M, Li Y, Ye W, et al. A CRISPR/Cas9-mediated in situ complementation method for phytophthora sojae mutants. Mol Plant Pathol. 2021;22(3):373–381. doi: 10.1111/mpp.13028
   PubMed Web of Science ®Google Scholar
• Fang Y, Cui L, Gu B, et al. Efficient genome editing in the Oomycete Phytophthora sojae using CRISPR/Cas9. Curr Protoc Microbiol. 2017;44(1):21–21A 21 26. doi: 10.1002/cpmc.25
   Google Scholar
• Livak KJ, Schmittgen TD. Analysis of relative gene expression data using Real-Time Quantitative PCR and the 2−ΔΔCT method. Methods. 2001;25(4):402–408. doi: 10.1006/meth.2001.1262
   PubMed Web of Science ®Google Scholar
• Huang J, Xi P, Deng Y, et al. The mitogen-activated protein kinase PlMAPK2 is involved in zoosporogenesis and pathogenicity of Peronophythora litchii. Int J Mol Sci. 2021;22(7):3524. doi: 10.3390/ijms22073524
   PubMed Web of Science ®Google Scholar
• Lin L, Ye W, Wu J, et al. The MADS-box transcription factor PsMAD1 is involved in zoosporogenesis and pathogenesis of Phytophthora sojae. Front Microbiol. 2018;9:2259. doi: 10.3389/fmicb.2018.02259
   PubMed Web of Science ®Google Scholar
• Contento AL, Xiong Y, Bassham DC. Visualization of autophagy in Arabidopsis using the fluorescent dye monodansylcadaverine and a GFP-AtATG8e fusion protein. Plant J. 2005;42(4):598–608. doi: 10.1111/j.1365-313X.2005.02396.x
   PubMed Web of Science ®Google Scholar
• Hardham AR. Cell biology of plant-oomycete interactions. Cell Microbiol. 2007;9(1):31–39. doi: 10.1111/j.1462-5822.2006.00833.x
   PubMed Web of Science ®Google Scholar
• Sun J, Gao Z, Zhang X, et al. Transcriptome analysis of Phytophthora litchii reveals pathogenicity arsenals and confirms taxonomic status. PloS One. 2017;12(6):e0178245. doi: 10.1371/journal.pone.0178245
   PubMed Web of Science ®Google Scholar
• Blanco FA, Judelson HS. A bZIP transcription factor from Phytophthora interacts with a protein kinase and is required for zoospore motility and plant infection. Mol Microbiol. 2005;56(3):638–648. doi: 10.1111/j.1365-2958.2005.04575.x
   PubMed Web of Science ®Google Scholar
• Judelson HS, Blanco FA. The spores of Phytophthora: weapons of the plant destroyer. Nat Rev Microbiol. 2005;3(1):47–58. doi: 10.1038/nrmicro1064
   PubMed Web of Science ®Google Scholar
• Shintani T, Suzuki K, Kamada Y, et al. Apg2p functions in autophagosome formation on the perivacuolar structure. J Biol Chem. 2001;276(32):30452–30460. doi: 10.1074/jbc.M102346200
   PubMed Web of Science ®Google Scholar
• Wang CW, Kim J, Huang WP, et al. Apg2 is a novel protein required for the cytoplasm to vacuole targeting, autophagy, and pexophagy pathways. J Biol Chem. 2001;276(32):30442–30451. doi: 10.1074/jbc.M102342200
   PubMed Web of Science ®Google Scholar
• Velikkakath AK, Nishimura T, Oita E, et al. Mammalian Atg2 proteins are essential for autophagosome formation and important for regulation of size and distribution of lipid droplets. MboC. 2012;23(5):896–909. doi: 10.1091/mbc.e11-09-0785
   Google Scholar
• Abeliovich H, Klionsky DJ. Autophagy in yeast: mechanistic insights and physiological function. Microbiol Mol Biol Rev. 2001;65(3):463–479. doi: 10.1128/MMBR.65.3.463-479.2001
   PubMed Web of Science ®Google Scholar
• Levine B, Klionsky DJ. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev Cell. 2004;6(4):463–477. doi: 10.1016/S1534-5807(04)00099-1
   PubMed Web of Science ®Google Scholar
• Meijer AJ, Codogno P. Regulation and role of autophagy in mammalian cells. Int J Biochem Cell Biol. 2004;36(12):2445–2462. doi: 10.1016/j.biocel.2004.02.002
   PubMed Web of Science ®Google Scholar
• Kikuma T, Kitamoto K. Analysis of autophagy in aspergillus oryzae by disruption of Aoatg13, Aoatg4, and Aoatg15 genes. FEMS Microbiol Lett. 2011;316(1):61–69. doi: 10.1111/j.1574-6968.2010.02192.x
   PubMed Web of Science ®Google Scholar
• Pollack JK, Harris SD, Marten MR. Autophagy in filamentous fungi. Fungal Genet Biol. 2009;46(1):1–8. doi: 10.1016/j.fgb.2008.10.010
   PubMed Web of Science ®Google Scholar
• Veneault-Fourrey C, Barooah M, Egan M, et al. Autophagic fungal cell death is necessary for infection by the rice blast fungus. Science. 2006;312(5773):580–583. doi: 10.1126/science.1124550
   PubMed Web of Science ®Google Scholar
• Liu XH, Liu TB, Lin FC. Monitoring autophagy in Magnaporthe oryzae. Methods Enzymol. 2008;451:271–294.
   PubMed Web of Science ®Google Scholar
• Shi H, Yang Z, Huang J, et al. An effector of ‘candidatus liberibacter asiaticus’ manipulates autophagy to promote bacterial infection. J Exp Bot erad176. 2023a;74(15):4670–4684. doi: 10.1093/jxb/erad176
   PubMed Web of Science ®Google Scholar
• Shi J, Gong Y, Shi H, et al. ‘Candidatus liberibacter asiaticus’ secretory protein SDE3 inhibits host autophagy to promote huanglongbing disease in citrus. Autophagy. 2023b;1–17. doi: 10.1080/15548627.2023.2278414
   Web of Science ®Google Scholar
• Testi S, ML K, Allasia V, et al. An oomycete effector impairs autophagy in evolutionary distant organisms and favors host infection. Cold Spring Harbor Lab. 2019;697136. doi:10.1101/697136
   Google Scholar
• Tyler BM. Phytophthora sojae: root rot pathogen of soybean and model oomycete. Mol Plant Pathol. 2007;8(1):1–8. doi: 10.1111/j.1364-3703.2006.00373.x
   PubMed Web of Science ®Google Scholar