Linking Autophagy to Potential Agronomic Trait Improvement in Crops
Abstract
:1. Introduction
2. The Role of Autophagy in Nutrient Recycling and Remobilization
2.1. The Acute Response of Autophagy to Nutrient Deprivation and Leaf Senescence
2.2. Autophagy-Dependent Recycling and Remobilization of Nitrogen
2.3. Autophagic Recycling and Remobilization of Micronutrients and Sulphur
2.4. The Autophagy-Dependent Remobilization of Carbonhydrates
2.5. Autophagy-Dependent Lipid Metabolism
3. The Role of Autophagy during Development
3.1. Vegetative Growth
3.2. Reproductive Development
4. The Role of Autophagy in the Responses to Abiotic Stress
4.1. Temperature Stress
4.2. Drought and Salinity Stress
4.3. Hypoxia or Oxidative Stress
5. The Role of Autophagy in Responses to Biotic Stress
5.1. Autophagy during Virus Infection
5.2. Autophagy during Fungi and Oomycete Infection
5.3. Autophagy during Bacterial Infection
6. Potential Approaches of Autophagy Manipulation for Crop Improvement
6.1. Genetic Manipulation of ATG Genes
6.2. Genetic Manipulation of Autophagy Regulators
6.3. Pharmacological Regulation
7. Future Perspectives
Author Contributions
Funding
Conflicts of Interest
References
- Rabinowitz, J.D.; White, E. Autophagy and metabolism. Science 2010, 330, 1344–1348. [Google Scholar] [CrossRef] [Green Version]
- Marshall, R.S.; Vierstra, R.D. Autophagy: The Master of Bulk and Selective Recycling. Annu. Rev. Plant Biol. 2018, 69, 173–208. [Google Scholar] [CrossRef]
- Yoshimoto, K.; Ohsumi, Y. Unveiling the Molecular Mechanisms of Plant Autophagy-From Autophagosomes to Vacuoles in Plants. Plant Cell Physiol. 2018, 59, 1337–1344. [Google Scholar] [CrossRef]
- Nakatogawa, H. Mechanisms governing autophagosome biogenesis. Nat. Rev. Mol. Cell Biol. 2020, 21, 439–458. [Google Scholar] [CrossRef]
- Hofius, D.; Li, L.; Hafren, A.; Coll, N.S. Autophagy as an emerging arena for plant-pathogen interactions. Curr. Opin. Plant Biol. 2017, 38, 117–123. [Google Scholar] [CrossRef]
- Tang, J.; Bassham, D.C. Autophagy in crop plants: What’s new beyond Arabidopsis? Open Biol. 2018, 8. [Google Scholar] [CrossRef] [Green Version]
- Zhou, X.; Zhao, P.; Sun, M.X. Autophagy in sexual plant reproduction: New insights. J. Exp. Bot. 2021, 72, 7658–7667. [Google Scholar] [CrossRef]
- Signorelli, S.; Tarkowski, L.P.; Van den Ende, W.; Bassham, D.C. Linking Autophagy to Abiotic and Biotic Stress Responses. Trends Plant Sci. 2019, 24, 413–430. [Google Scholar] [CrossRef] [Green Version]
- Masclaux-Daubresse, C.; Chen, Q.; Have, M. Regulation of nutrient recycling via autophagy. Curr. Opin. Plant Biol. 2017, 39, 8–17. [Google Scholar] [CrossRef]
- Hanaoka, H.; Noda, T.; Shirano, Y.; Kato, T.; Hayashi, H.; Shibata, D.; Tabata, S.; Ohsumi, Y. Leaf senescence and starvation-induced chlorosis are accelerated by the disruption of an Arabidopsis autophagy gene. Plant Physiol. 2002, 129, 1181–1193. [Google Scholar] [CrossRef] [Green Version]
- Yoshimoto, K.; Hanaoka, H.; Sato, S.; Kato, T.; Tabata, S.; Noda, T.; Ohsumi, Y. Processing of ATG8s, ubiquitin-like proteins, and their deconjugation by ATG4s are essential for plant autophagy. Plant Cell 2004, 16, 2967–2983. [Google Scholar] [CrossRef]
- Li, F.; Chung, T.; Vierstra, R.D. AUTOPHAGY-RELATED11 plays a critical role in general autophagy- and senescence-induced mitophagy in Arabidopsis. Plant Cell 2014, 26, 788–807. [Google Scholar] [CrossRef] [Green Version]
- Li, F.; Chung, T.; Pennington, J.G.; Federico, M.L.; Kaeppler, H.F.; Kaeppler, S.M.; Otegui, M.S.; Vierstra, R.D. Autophagic recycling plays a central role in maize nitrogen remobilization. Plant Cell 2015, 27, 1389–1408. [Google Scholar] [CrossRef] [Green Version]
- Liu, F.; Hu, W.; Li, F.; Marshall, R.S.; Zarza, X.; Munnik, T.; Vierstra, R.D. AUTOPHAGY-RELATED14 and Its Associated Phosphatidylinositol 3-Kinase Complex Promote Autophagy in Arabidopsis. Plant Cell 2020, 32, 3939–3960. [Google Scholar] [CrossRef]
- Guiboileau, A.; Yoshimoto, K.; Soulay, F.; Bataille, M.P.; Avice, J.C.; Masclaux-Daubresse, C. Autophagy machinery controls nitrogen remobilization at the whole-plant level under both limiting and ample nitrate conditions in Arabidopsis. New Phytol. 2012, 194, 732–740. [Google Scholar] [CrossRef]
- Chung, T.; Phillips, A.R.; Vierstra, R.D. ATG8 lipidation and ATG8-mediated autophagy in Arabidopsis require ATG12 expressed from the differentially controlled ATG12A AND ATG12B loci. Plant J. 2010, 62, 483–493. [Google Scholar] [CrossRef]
- Doelling, J.H.; Walker, J.M.; Friedman, E.M.; Thompson, A.R.; Vierstra, R.D. The APG8/12-activating enzyme APG7 is required for proper nutrient recycling and senescence in Arabidopsis thaliana. J. Biol. Chem. 2002, 277, 33105–33114. [Google Scholar] [CrossRef] [Green Version]
- Phillips, A.R.; Suttangkakul, A.; Vierstra, R.D. The ATG12-conjugating enzyme ATG10 is essential for autophagic vesicle formation in Arabidopsis thaliana. Genetics 2008, 178, 1339–1353. [Google Scholar] [CrossRef] [Green Version]
- Thompson, A.R.; Doelling, J.H.; Suttangkakul, A.; Vierstra, R.D. Autophagic nutrient recycling in Arabidopsis directed by the ATG8 and ATG12 conjugation pathways. Plant Physiol. 2005, 138, 2097–2110. [Google Scholar] [CrossRef] [Green Version]
- Xiong, Y.; Contento, A.L.; Bassham, D.C. AtATG18a is required for the formation of autophagosomes during nutrient stress and senescence in Arabidopsis thaliana. Plant J. 2005, 42, 535–546. [Google Scholar] [CrossRef]
- Suttangkakul, A.; Li, F.Q.; Chung, T.; Vierstra, R.D. The ATG1/ATG13 Protein Kinase Complex Is Both a Regulator and a Target of Autophagic Recycling in Arabidopsis. Plant Cell 2011, 23, 3761–3779. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Naumann, C.; Muller, J.; Sakhonwasee, S.; Wieghaus, A.; Hause, G.; Heisters, M.; Burstenbinder, K.; Abel, S. The Local Phosphate Deficiency Response Activates Endoplasmic Reticulum Stress-Dependent Autophagy (vol 179, pg 460, 2019). Plant Physiol. 2020, 184, 2240–2241. [Google Scholar] [CrossRef] [Green Version]
- Eguchi, M.; Kimura, K.; Makino, A.; Ishida, H. Autophagy is induced under Zn limitation and contributes to Zn-limited stress tolerance in Arabidopsis (Arabidopsis thaliana). Soil Sci. Plant Nutr. 2017, 63, 342–350. [Google Scholar] [CrossRef] [Green Version]
- Dong, Y.H.; Silbermann, M.; Speiser, A.; Forieri, I.; Linster, E.; Poschet, G.; Samami, A.A.; Wanatabe, M.; Sticht, C.; Teleman, A.A.; et al. Sulfur availability regulates plant growth via glucose-TOR signaling. Nat. Commun. 2017, 8. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shinozaki, D.; Merkulova, E.A.; Naya, L.; Horie, T.; Kanno, Y.; Seo, M.; Ohsumi, Y.; Masclaux-Daubresse, C.; Yoshimoto, K. Autophagy Increases Zinc Bioavailability to Avoid Light-Mediated Reactive Oxygen Species Production under Zinc Deficiency(1)([OPEN]). Plant Physiol. 2020, 182, 1284–1296. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lornac, A.; Have, M.; Chardon, F.; Soulay, F.; Clement, G.; Avice, J.C.; Masclaux-Daubresse, C. Autophagy Controls Sulphur Metabolism in the Rosette Leaves of Arabidopsis and Facilitates S Remobilization to the Seeds. Cells 2020, 9, 332. [Google Scholar] [CrossRef] [PubMed]
- Xia, K.; Liu, T.; Ouyang, J.; Wang, R.; Fan, T.; Zhang, M. Genome-wide identification, classification, and expression analysis of autophagy-associated gene homologues in rice (Oryza sativa L.). DNA Res. 2011, 18, 363–377. [Google Scholar] [CrossRef] [Green Version]
- Izumi, M.; Hidema, J.; Wada, S.; Kondo, E.; Kurusu, T.; Kuchitsu, K.; Makino, A.; Ishida, H. Establishment of monitoring methods for autophagy in rice reveals autophagic recycling of chloroplasts and root plastids during energy limitation. Plant Physiol. 2015, 167, 1307–1320. [Google Scholar] [CrossRef] [Green Version]
- Zhai, Y.; Guo, M.; Wang, H.; Lu, J.; Liu, J.; Zhang, C.; Gong, Z.; Lu, M. Autophagy, a Conserved Mechanism for Protein Degradation, Responds to Heat, and Other Abiotic Stresses in Capsicum annuum L. Front. Plant Sci. 2016, 7, 131. [Google Scholar] [CrossRef] [Green Version]
- Chung, T.; Suttangkakul, A.; Vierstra, R.D. 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. 2009, 149, 220–234. [Google Scholar] [CrossRef] [Green Version]
- Zeng, X.W.; Zeng, Z.H.; Liu, C.C.; Yuan, W.Y.; Hou, N.; Bian, H.W.; Zhu, M.Y.; Han, N. A barley homolog of yeast ATG6 is involved in multiple abiotic stress responses and stress resistance regulation. Plant Physiol. Bioch. 2017, 115, 97–106. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xia, T.; Xiao, D.; Liu, D.; Chai, W.; Gong, Q.; Wang, N.N. Heterologous expression of ATG8c from soybean confers tolerance to nitrogen deficiency and increases yield in Arabidopsis. PLoS ONE 2012, 7, e37217. [Google Scholar] [CrossRef] [PubMed]
- Li, W.W.; Chen, M.; Wang, E.H.; Hu, L.Q.; Hawkesford, M.J.; Zhong, L.; Chen, Z.; Xu, Z.S.; Li, L.C.; Zhou, Y.B.; et al. 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 Genom. 2016, 17. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wada, S.; Hayashida, Y.; Izumi, M.; Kurusu, T.; Hanamata, S.; Kanno, K.; Kojima, S.; Yamaya, T.; Kuchitsu, K.; Makino, A.; et al. Autophagy Supports Biomass Production and Nitrogen Use Efficiency at the Vegetative Stage in Rice. Plant Physiol. 2015, 168, 60–73. [Google Scholar] [CrossRef] [Green Version]
- Kurusu, T.; Koyano, T.; Hanamata, S.; Kubo, T.; Noguchi, Y.; Yagi, C.; Nagata, N.; Yamamoto, T.; Ohnishi, T.; Okazaki, Y.; et al. OsATG7 is required for autophagy-dependent lipid metabolism in rice postmeiotic anther development. Autophagy 2014, 10, 878–888. [Google Scholar] [CrossRef]
- Avila-Ospina, L.; Moison, M.; Yoshimoto, K.; Masclaux-Daubresse, C. Autophagy, plant senescence, and nutrient recycling. J. Exp. Bot. 2014, 65, 3799–3811. [Google Scholar] [CrossRef] [Green Version]
- Gregersen, P.L.; Culetic, A.; Boschian, L.; Krupinska, K. Plant senescence and crop productivity. Plant Mol. Biol. 2013, 82, 603–622. [Google Scholar] [CrossRef]
- Breeze, E.; Harrison, E.; McHattie, S.; Hughes, L.; Hickman, R.; Hill, C.; Kiddle, S.; Kim, Y.S.; Penfold, C.A.; Jenkins, D.; et al. High-Resolution Temporal Profiling of Transcripts during Arabidopsis Leaf Senescence Reveals a Distinct Chronology of Processes and Regulation. Plant Cell 2011, 23, 873–894. [Google Scholar] [CrossRef] [Green Version]
- Masclaux-Daubresse, C.; Daniel-Vedele, F.; Dechorgnat, J.; Chardon, F.; Gaufichon, L.; Suzuki, A. Nitrogen uptake, assimilation and remobilization in plants: Challenges for sustainable and productive agriculture. Ann. Bot. 2010, 105, 1141–1157. [Google Scholar] [CrossRef] [Green Version]
- Wang, P.; Sun, X.; Jia, X.; Wang, N.; Gong, X.Q.; Ma, F.W. Characterization of an Autophagy-Related Gene MdATG8i from Apple. Front. Plant Sci. 2016, 7. [Google Scholar] [CrossRef] [Green Version]
- Htwe, N.M.P.S.; Yuasa, T.; Ishibashi, Y.; Tanigawa, H.; Okuda, M.; Zheng, S.H.; Iwaya-Inoue, M. Leaf Senescence of Soybean at Reproductive Stage is Associated with Induction of Autophagy-related Genes, GmATG8c, GmATG8i and GmATG4. Plant Prod. Sci. 2011, 14, 141–147. [Google Scholar] [CrossRef] [Green Version]
- Islam, M.M.; Ishibashi, Y.; Nakagawa, A.C.S.; Tomita, Y.; Iwaya-Inoue, M.; Arima, S.; Zheng, S.H. Nitrogen redistribution and its relationship with the expression of GmATG8c during seed filling in soybean. J. Plant Physiol. 2016, 192, 71–74. [Google Scholar] [CrossRef] [PubMed]
- Hollmann, J.; Gregersen, P.L.; Krupinska, K. Identification of predominant genes involved in regulation and execution of senescence-associated nitrogen remobilization in flag leaves of field grown barley. J. Exp. Bot. 2014, 65, 3963–3973. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Guiboileau, A.; Avila-Ospina, L.; Yoshimoto, K.; Soulay, F.; Azzopardi, M.; Marmagne, A.; Lothier, J.; Masclaux-Daubresse, C. Physiological and metabolic consequences of autophagy deficiency for the management of nitrogen and protein resources in Arabidopsis leaves depending on nitrate availability. New Phytol. 2013, 199, 683–694. [Google Scholar] [CrossRef] [PubMed]
- Li, W.W.; Chen, M.; Zhong, L.; Liu, J.M.; Xu, Z.S.; Li, L.C.; Zhou, Y.B.; Guo, C.H.; Ma, Y.Z. 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. Bioph. Res. Co. 2015, 468, 800–806. [Google Scholar] [CrossRef] [PubMed]
- Wang, P.; Sun, X.; Jia, X.; Ma, F. Apple autophagy-related protein MdATG3s afford tolerance to multiple abiotic stresses. Plant Sci. 2017, 256, 53–64. [Google Scholar] [CrossRef] [PubMed]
- Huo, L.; Guo, Z.; Zhang, Z.; Jia, X.; Sun, Y.; Sun, X.; Wang, P.; Gong, X.; Ma, F. The Apple Autophagy-Related Gene MdATG9 Confers Tolerance to Low Nitrogen in Transgenic Apple Callus. Front. Plant Sci. 2020, 11, 423. [Google Scholar] [CrossRef] [Green Version]
- Sun, X.; Jia, X.; Huo, L.Q.; Che, R.M.; Gong, X.Q.; Wang, P.; Ma, F.W. MdATG18a overexpression improves tolerance to nitrogen deficiency and regulates anthocyanin accumulation through increased autophagy in transgenic apple. Plant Cell Environ. 2018, 41, 469–480. [Google Scholar] [CrossRef]
- Yu, J.; Zhen, X.; Li, X.; Li, N.; Xu, F. Increased Autophagy of Rice Can Increase Yield and Nitrogen Use Efficiency (NUE). Front. Plant Sci. 2019, 10, 584. [Google Scholar] [CrossRef] [Green Version]
- Zhen, X.; Li, X.; Yu, J.; Xu, F. OsATG8c-Mediated Increased Autophagy Regulates the Yield and Nitrogen Use Efficiency in Rice. Int. J. Mol. Sci. 2019, 20, 4956. [Google Scholar] [CrossRef] [Green Version]
- Fan, T.; Yang, W.; Zeng, X.; Xu, X.L.; Xu, Y.L.; Fan, X.R.; Luo, M.; Tian, C.G.; Xia, K.F.; Zhang, M.Y. A Rice Autophagy Gene OsATG8b Is Involved in Nitrogen Remobilization and Control of Grain Quality. Front. Plant Sci. 2020, 11. [Google Scholar] [CrossRef] [PubMed]
- Zhen, X.; Zheng, N.; Yu, J.; Bi, C.; Xu, F. Autophagy mediates grain yield and nitrogen stress resistance by modulating nitrogen remobilization in rice. PLoS ONE 2021, 16, e0244996. [Google Scholar] [CrossRef] [PubMed]
- Pottier, M.; Dumont, J.; Masclaux-Daubresse, C.; Thomine, S. Autophagy is essential for optimal translocation of iron to seeds in Arabidopsis. J. Exp. Bot. 2019, 70, 859–869. [Google Scholar] [CrossRef] [Green Version]
- Sulpice, R.; Pyl, E.T.; Ishihara, H.; Trenkamp, S.; Steinfath, M.; Witucka-Wall, H.; Gibon, Y.; Usadel, B.; Poree, F.; Piques, M.C.; et al. Starch as a major integrator in the regulation of plant growth. Proc. Natl. Acad. Sci. USA 2009, 106, 10348–10353. [Google Scholar] [CrossRef] [Green Version]
- Wang, Y.; Yu, B.; Zhao, J.; Guo, J.; Li, Y.; Han, S.; Huang, L.; Du, Y.; Hong, Y.; Tang, D.; et al. Autophagy contributes to leaf starch degradation. Plant Cell 2013, 25, 1383–1399. [Google Scholar] [CrossRef] [Green Version]
- Wang, Y.; Liu, Y. Autophagic degradation of leaf starch in plants. Autophagy 2013, 9, 1247–1248. [Google Scholar] [CrossRef] [Green Version]
- Ren, C.; Liu, J.; Gong, Q. Functions of autophagy in plant carbon and nitrogen metabolism. Front. Plant Sci. 2014, 5, 301. [Google Scholar] [CrossRef] [Green Version]
- Izumi, M.; Hidema, J.; Makino, A.; Ishida, H. Autophagy contributes to nighttime energy availability for growth in Arabidopsis. Plant Physiol. 2013, 161, 1682–1693. [Google Scholar] [CrossRef] [Green Version]
- McLoughlin, F.; Augustine, R.C.; Marshall, R.S.; Li, F.Q.; Kirkpatrick, L.D.; Otegui, M.S.; Vierstra, R.D. Maize multi-omics reveal roles for autophagic recycling in proteome remodelling and lipid turnover. Nat. Plants 2018, 4, 1056–1070. [Google Scholar] [CrossRef]
- McLoughlin, F.; Marshall, R.S.; Ding, X.; Chatt, E.C.; Kirkpatrick, L.D.; Augustine, R.C.; Li, F.; Otegui, M.S.; Vierstra, R.D. Autophagy Plays Prominent Roles in Amino Acid, Nucleotide, and Carbohydrate Metabolism during Fixed-Carbon Starvation in Maize. Plant Cell 2020, 32, 2699–2724. [Google Scholar] [CrossRef]
- Han, B.; Xu, H.; Feng, Y.T.; Xu, W.; Cui, Q.H.; Liu, A.Z. Genomic Characterization and Expressional Profiles of Autophagy-Related Genes (ATGs) in Oilseed Crop Castor Bean (Ricinus communis L.). Int. J. Mol. Sci. 2020, 21, 562. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Masclaux-Daubresse, C.; Clement, G.; Anne, P.; Routaboul, J.M.; Guiboileau, A.; Soulay, F.; Shirasu, K.; Yoshimoto, K. Stitching together the Multiple Dimensions of Autophagy Using Metabolomics and Transcriptomics Reveals Impacts on Metabolism, Development, and Plant Responses to the Environment in Arabidopsis. Plant Cell 2014, 26, 1857–1877. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yoshimoto, K.; Jikumaru, Y.; Kamiya, Y.; Kusano, M.; Consonni, C.; Panstruga, R.; Ohsumi, Y.; Shirasu, K. 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, 2914–2927. [Google Scholar] [CrossRef] [Green Version]
- Jia, M.; Liu, X.Y.; Xue, H.; Wu, Y.; Shi, L.; Wang, R.; Chen, Y.; Xu, N.; Zhao, J.; Shao, J.X.; et al. Noncanonical ATG8-ABS3 interaction controls senescence in plants. Nat. Plants 2019, 5, 212–224. [Google Scholar] [CrossRef] [PubMed]
- Feng, X.; Liu, L.L.; Li, Z.G.; Sun, F.; Wu, X.Y.; Hao, D.Y.; Hao, H.Q.; Jing, H.C. Potential interaction between autophagy and auxin during maize leaf senescence. J. Exp. Bot. 2021, 72, 3554–3568. [Google Scholar] [CrossRef] [PubMed]
- Deb, S.; Sankaranarayanan, S.; Wewala, G.; Widdup, E.; Samuel, M.A. The S-Domain Receptor Kinase Arabidopsis Receptor Kinase2 and the U Box/Armadillo Repeat-Containing E3 Ubiquitin Ligase9 Module Mediates Lateral Root Development under Phosphate Starvation in Arabidopsis. Plant Physiol. 2014, 165, 1647–1656. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Harrison-Lowe, N.J.; Olsen, L.J. Autophagy protein 6 (ATG6) is required for pollen germination in Arabidopsis thaliana. Autophagy 2008, 4, 339–348. [Google Scholar] [CrossRef] [Green Version]
- Sankaranarayanan, S.; Samuel, M.A. A proposed role for selective autophagy in regulating auxin-dependent lateral root development under phosphate starvation in Arabidopsis. Plant Signal. Behav. 2015, 10. [Google Scholar] [CrossRef] [Green Version]
- Zhao, P.; Zhou, X.M.; Zhao, L.L.; Cheung, A.Y.; Sun, M.X. Autophagy-mediated compartmental cytoplasmic deletion is essential for tobacco pollen germination and male fertility. Autophagy 2020, 16, 2180–2192. [Google Scholar] [CrossRef]
- Norizuki, T.; Minamino, N.; Ueda, T. Role of Autophagy in Male Reproductive Processes in Land Plants. Front. Plant. Sci. 2020, 11, 756. [Google Scholar] [CrossRef]
- Huang, L.; Yu, L.J.; Zhang, X.; Fan, B.; Wang, F.Z.; Dai, Y.S.; Qi, H.; Zhou, Y.; Xie, L.J.; Xiao, S. Autophagy regulates glucose-mediated root meristem activity by modulating ROS production in Arabidopsis. Autophagy 2019, 15, 407–422. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xiong, Y.; McCormack, M.; Li, L.; Hall, Q.; Xiang, C.; Sheen, J. Glucose-TOR signalling reprograms the transcriptome and activates meristems. Nature 2013, 496, 181–186. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Deng, K.X.; Dong, P.; Wang, W.J.; Feng, L.; Xiong, F.J.; Wang, K.; Zhang, S.M.; Feng, S.; Wang, B.J.; Zhang, J.K.; et al. The TOR Pathway Is Involved in Adventitious Root Formation in Arabidopsis and Potato. Front. Plant Sci. 2017, 8. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Qin, G.J.; Ma, Z.Q.; Zhang, L.; Xing, S.F.; Hou, X.H.; Deng, J.; Liu, J.L.; Chen, Z.L.; Qu, L.J.; Gu, H.Y. Arabidopsis AtBECLIN 1/AtAtg6/AtVps30 is essential for pollen germination and plant development. Cell Res. 2007, 17, 249–263. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fujiki, Y.; Yoshimoto, K.; Ohsumi, Y. An Arabidopsis homolog of yeast ATG6/VPS30 is essential for pollen germination. Plant Physiol. 2007, 143, 1132–1139. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kurusu, T.; Koyano, T.; Kitahata, N.; Kojima, M.; Hanamata, S.; Sakakibara, H.; Kuchitsu, K. Autophagy-mediated regulation of phytohormone metabolism during rice anther development. Plant Signal. Behav. 2017, 12. [Google Scholar] [CrossRef] [PubMed]
- Ghiglione, H.O.; Gonzalez, F.G.; Serrago, R.; Maldonado, S.B.; Chilcott, C.; Cura, J.A.; Miralles, D.J.; Zhu, T.; Casal, J.J. Autophagy regulated by day length determines the number of fertile florets in wheat. Plant J. 2008, 55, 1010–1024. [Google Scholar] [CrossRef]
- Barros, J.A.S.; Cavalcanti, J.H.F.; Medeiros, D.B.; Nunes-Nesi, A.; Avin-Wittenberg, T.; Fernie, A.R.; Araujo, W.L. Autophagy Deficiency Compromises Alternative Pathways of Respiration following Energy Deprivation in Arabidopsis thaliana. Plant Physiol. 2017, 175, 62–76. [Google Scholar] [CrossRef] [Green Version]
- Minina, E.A.; Moschou, P.N.; Vetukuri, R.R.; Sanchez-Vera, V.; Cardoso, C.; Liu, Q.S.; Elander, P.H.; Dalman, K.; Beganovic, M.; Yilmaz, J.L.; et al. Transcriptional stimulation of rate-limiting components of the autophagic pathway improves plant fitness. J. Exp. Bot. 2018, 69, 1415–1432. [Google Scholar] [CrossRef]
- Sera, Y.; Hanamata, S.; Sakamoto, S.; Ono, S.; Kaneko, K.; Mitsui, Y.; Koyano, T.; Fujita, N.; Sasou, A.; Masumura, T.; et al. Essential roles of autophagy in metabolic regulation in endosperm development during rice seed maturation. Sci. Rep. 2019, 9, 18544. [Google Scholar] [CrossRef] [Green Version]
- Li, Y.B.; Yan, M.; Cui, D.Z.; Huang, C.; Sui, X.X.; Guo, F.Z.; Fan, Q.Q.; Chu, X.S. Programmed Degradation of Pericarp Cells in Wheat Grains Depends on Autophagy. Front. Genet. 2021, 12. [Google Scholar] [CrossRef] [PubMed]
- Sanchez-Sevilla, J.F.; Botella, M.A.; Valpuesta, V.; Sanchez-Vera, V. Autophagy Is Required for Strawberry Fruit Ripening. Front. Plant Sci. 2021, 12. [Google Scholar] [CrossRef] [PubMed]
- Ghan, R.; Petereit, J.; Tillett, R.L.; Schlauch, K.A.; Toubiana, D.; Fait, A.; Cramer, G.R. The common transcriptional subnetworks of the grape berry skin in the late stages of ripening. Bmc Plant Biol. 2017, 17. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chi, C.; Li, X.M.; Fang, P.P.; Xia, X.J.; Shi, K.; Zhou, Y.H.; Zhou, J.; Yu, J.Q. Brassinosteroids act as a positive regulator of NBR1-dependent selective autophagy in response to chilling stress in tomato. J. Exp. Bot. 2020, 71, 1092–1106. [Google Scholar] [CrossRef] [PubMed]
- Chen, L.; Liao, B.; Qi, H.; Xie, L.J.; Huang, L.; Tan, W.J.; Zhai, N.; Yuan, L.B.; Zhou, Y.; Yu, L.J.; et al. Autophagy contributes to regulation of the hypoxia response during submergence in Arabidopsis thaliana. Autophagy 2015, 11, 2233–2246. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhou, J.; Wang, J.; Cheng, Y.; Chi, Y.J.; Fan, B.F.; Yu, J.Q.; Chen, Z.X. NBR1-Mediated Selective Autophagy Targets Insoluble Ubiquitinated Protein Aggregates in Plant Stress Responses. Plos Genet. 2013, 9. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, Y.M.; Xiong, Y.; Bassham, D.C. Autophagy is required for tolerance of drought and salt stress in plants. Autophagy 2009, 5, 954–963. [Google Scholar] [CrossRef] [Green Version]
- Xiong, Y.; Contento, A.L.; Nguyen, P.Q.; Bassham, D.C. Degradation of oxidized proteins by autophagy during oxidative stress in Arabidopsis. Plant Physiol. 2007, 143, 291–299. [Google Scholar] [CrossRef] [Green Version]
- Wang, Y.; Cai, S.; Yin, L.; Shi, K.; Xia, X.; Zhou, Y.; Yu, J.; Zhou, J. Tomato HsfA1a plays a critical role in plant drought tolerance by activating ATG genes and inducing autophagy. Autophagy 2015, 11, 2033–2047. [Google Scholar] [CrossRef] [Green Version]
- Sun, X.; Wang, P.; Jia, X.; Huo, L.; Che, R.; Ma, F. Improvement of drought tolerance by overexpressing MdATG18a is mediated by modified antioxidant system and activated autophagy in transgenic apple. Plant Biotechnol. J. 2018, 16, 545–557. [Google Scholar] [CrossRef] [Green Version]
- Li, Y.B.; Cui, D.Z.; Sui, X.X.; Huang, C.; Huang, C.Y.; Fan, Q.Q.; Chu, X.S. Autophagic Survival Precedes Programmed Cell Death in Wheat Seedlings Exposed to Drought Stress. Int. J. Mol. Sci. 2019, 20, 5777. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, J.Z.; Yang, W.W.; Yue, J.Y.; Liu, Y.N.; Pei, D.; Wang, H.Z. The Responses of Wheat Autophagy and ATG8 Family Genes to Biotic and Abiotic Stresses. J. Plant Growth Regul. 2020, 39, 867–876. [Google Scholar] [CrossRef]
- Zhou, J.; Wang, J.; Yu, J.Q.; Chen, Z.X. Role and regulation of autophagy in heat stress responses of tomato plants. Front. Plant Sci. 2014, 5. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhou, L.L.; Gao, K.Y.; Cheng, L.S.; Wang, Y.L.; Cheng, Y.K.; Xu, Q.T.; Deng, X.Y.; Li, J.W.; Mei, F.Z.; Zhou, Z.Q. Short-term waterlogging-induced autophagy in root cells of wheat can inhibit programmed cell death. Protoplasma 2021, 258, 891–904. [Google Scholar] [CrossRef]
- Yue, J.Y.; Wang, Y.J.; Jiao, J.L.; Wang, H.Z. Silencing of ATG2 and ATG7 promotes programmed cell death in wheat via inhibition of autophagy under salt stress. Ecotox. Environ. Safe 2021, 225. [Google Scholar] [CrossRef]
- Pei, D.; Zhang, W.; Sun, H.; Wei, X.; Yue, J.; Wang, H. 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. 2014, 33, 1697–1710. [Google Scholar] [CrossRef]
- Kuzuoglu-Ozturk, D.; Cebeci Yalcinkaya, O.; Akpinar, B.A.; Mitou, G.; Korkmaz, G.; Gozuacik, D.; Budak, H. Autophagy-related gene, TdAtg8, in wild emmer wheat plays a role in drought and osmotic stress response. Planta 2012, 236, 1081–1092. [Google Scholar] [CrossRef]
- Sun, X.; Pan, B.S.; Xu, W.Y.; Chen, Q.M.; Wang, Y.; Ban, Q.Y.; Xing, C.H.; Zhang, S.L. Genome-wide identification and expression analysis of the pear autophagy-related gene PbrATG8 and functional verification of PbrATG8c in Pyrus bretschneideri Rehd. Planta 2021, 253. [Google Scholar] [CrossRef]
- Xu, W.; Cai, S.Y.; Zhang, Y.; Wang, Y.; Ahammed, G.J.; Xia, X.J.; Shi, K.; Zhou, Y.H.; Yu, J.Q.; Reiter, R.J.; et al. Melatonin enhances thermotolerance by promoting cellular protein protection in tomato plants. J. Pineal Res. 2016, 61, 457–469. [Google Scholar] [CrossRef]
- Valitova, J.; Renkova, A.; Mukhitova, F.; Dmitrieva, S.; Beckett, R.P.; Minibayeva, F.V. Membrane sterols and genes of sterol biosynthesis are involved in the response of Triticum aestivum seedlings to cold stress. Plant Physiol. Biochem. 2019, 142, 452–459. [Google Scholar] [CrossRef]
- Zhu, T.; Zou, L.J.; Li, Y.; Yao, X.H.; Xu, F.; Deng, X.G.; Zhang, D.W.; Lin, H.H. Mitochondrial alternative oxidase-dependent autophagy involved in ethylene-mediated drought tolerance in Solanum lycopersicum. Plant Biotechnol. J. 2018, 16, 2063–2076. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, X.; Liu, Q.W.; Feng, H.; Deng, J.; Zhang, R.X.; Wen, J.Q.; Dong, J.L.; Wang, T. Dehydrin MtCAS31 promotes autophagic degradation under drought stress. Autophagy 2020, 16, 862–877. [Google Scholar] [CrossRef] [PubMed]
- Jia, X.; Mao, K.; Wang, P.; Wang, Y.; Jia, X.M.; Huo, L.Q.; Sun, X.; Che, R.M.; Gong, X.Q.; Ma, F.W. Overexpression of MdATG8i improves water use efficiency in transgenic apple by modulating photosynthesis, osmotic balance, and autophagic activity under moderate water deficit. Hortic Res.-England 2021, 8. [Google Scholar] [CrossRef] [PubMed]
- Huo, L.Q.; Guo, Z.J.; Wang, P.; Zhang, Z.J.; Jia, X.; Sun, Y.M.; Sun, X.; Gong, X.Q.; Ma, F.W. MdATG8i functions positively in apple salt tolerance by maintaining photosynthetic ability and increasing the accumulation of arginine and polyamines. Environ. Exp. Bot. 2020, 172. [Google Scholar] [CrossRef]
- Shin, J.H.; Yoshimoto, K.; Ohsumi, Y.; Jeon, J.S.; An, G. OsATG10b, an Autophagosome Component, Is Needed for Cell Survival against Oxidative Stresses in Rice. Mol. Cells 2009, 27, 67–74. [Google Scholar] [CrossRef]
- Lin, Z.; Wang, Y.L.; Cheng, L.S.; Zhou, L.L.; Xu, Q.T.; Liu, D.C.; Deng, X.Y.; Mei, F.Z.; Zhou, Z.Q. Mutual regulation of ROS accumulation and cell autophagy in wheat roots under hypoxia stress. Plant Physiol. Bioch. 2021, 158, 91–102. [Google Scholar] [CrossRef]
- Haxim, Y.; Ismayil, A.; Jia, Q.; Wang, Y.; Zheng, X.Y.; Chen, T.Y.; Qian, L.C.; Liu, N.; Wang, Y.J.; Han, S.J.; et al. Autophagy functions as an antiviral mechanism against geminiviruses in plants. Elife 2017, 6. [Google Scholar] [CrossRef]
- Hafren, A.; Macia, J.L.; Love, A.J.; Milner, J.J.; Drucker, M.; Hofius, D. Selective autophagy limits cauliflower mosaic virus infection by NBR1-mediated targeting of viral capsid protein and particles. Proc. Natl. Acad. Sci. USA 2017, 114, E2026–E2035. [Google Scholar] [CrossRef] [Green Version]
- Li, F.; Zhang, C.; Li, Y.; Wu, G.; Hou, X.; Zhou, X.; Wang, A. Beclin1 restricts RNA virus infection in plants through suppression and degradation of the viral polymerase. Nat. Commun. 2018, 9, 1268. [Google Scholar] [CrossRef]
- Hafren, A.; Ustun, S.; Hochmuth, A.; Svenning, S.; Johansen, T.; Hofius, D. Turnip Mosaic Virus Counteracts Selective Autophagy of the Viral Silencing Suppressor HCpro. Plant Physiol. 2018, 176, 649–662. [Google Scholar] [CrossRef] [Green Version]
- Yang, M.; Zhang, Y.; Xie, X.; Yue, N.; Li, J.; Wang, X.B.; Han, C.; Yu, J.; Liu, Y.; Li, D. Barley stripe mosaic virus gammab Protein Subverts Autophagy to Promote Viral Infection by Disrupting the ATG7-ATG8 Interaction. Plant Cell 2018, 30, 1582–1595. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jiang, L.; Lu, Y.; Zheng, X.; Yang, X.; Chen, Y.; Zhang, T.; Zhao, X.; Wang, S.; Zhao, X.; Song, X.; et al. The plant protein NbP3IP directs degradation of Rice stripe virus p3 silencing suppressor protein to limit virus infection through interaction with the autophagy-related protein NbATG8. New Phytol. 2021, 229, 1036–1051. [Google Scholar] [CrossRef] [PubMed]
- Shukla, A.; Hoffmann, G.; Kushwaha, N.K.; Lopez-Gonzalez, S.; Hofius, D.; Hafren, A. Salicylic acid and the viral virulence factor 2b regulate the divergent roles of autophagy during cucumber mosaic virus infection. Autophagy 2021, 1–13. [Google Scholar] [CrossRef]
- Jiao, Y.; An, M.; Li, X.; Yu, M.; Zhao, X.; Xia, Z.; Wu, Y. Transcriptomic and functional analyses reveal an antiviral role of autophagy during pepper mild mottle virus infection. BMC Plant Biol. 2020, 20, 495. [Google Scholar] [CrossRef] [PubMed]
- Yang, M.; Ismayil, A.; Liu, Y.L. Autophagy in Plant-Virus Interactions. Annu. Rev. Virol. 2020, 7, 403–419. [Google Scholar] [CrossRef] [PubMed]
- Ismayil, A.; Yang, M.; Liu, Y.L. Role of autophagy during plant-virus interactions. Semin. Cell Dev. Biol. 2020, 101, 36–40. [Google Scholar] [CrossRef] [PubMed]
- Kushwaha, N.K.; Hafrn, A.; Hofius, D. Autophagy-virus interplay in plants: From antiviral recognition to proviral manipulation. Mol. Plant Pathol. 2019, 20, 1211–1216. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lai, Z.; Wang, F.; Zheng, Z.; Fan, B.; Chen, Z. A critical role of autophagy in plant resistance to necrotrophic fungal pathogens. Plant J 2011, 66, 953–968. [Google Scholar] [CrossRef]
- Kabbage, M.; Williams, B.; Dickman, M.B. Cell Death Control: The Interplay of Apoptosis and Autophagy in the Pathogenicity of Sclerotinia sclerotiorum. Plos Pathog. 2013, 9. [Google Scholar] [CrossRef] [Green Version]
- Lenz, H.D.; Haller, E.; Melzer, E.; Kober, K.; Wurster, K.; Stahl, M.; Bassham, D.C.; Vierstra, R.D.; Parker, J.E.; Bautor, J.; et al. Autophagy differentially controls plant basal immunity to biotrophic and necrotrophic pathogens. Plant J. 2011, 66, 818–830. [Google Scholar] [CrossRef]
- Wang, Y.P.; Nishimura, M.T.; Zhao, T.; Tang, D.Z. ATG2, an autophagy-related protein, negatively affects powdery mildew resistance and mildew-induced cell death in Arabidopsis. Plant J. 2011, 68, 74–87. [Google Scholar] [CrossRef] [PubMed]
- Abdullah-Al Mamun, M.; Tang, C.L.; Sun, Y.C.; Islam, M.N.; Liu, P.; Wang, X.J.; Kang, Z.S. Wheat Gene TaATG8j Contributes to Stripe Rust Resistance. Int. J. Mol. Sci. 2018, 19, 1666. [Google Scholar] [CrossRef] [Green Version]
- Yue, J.Y.; Sun, H.; Zhang, W.; Pei, D.; He, Y.; Wang, H.Z. Wheat homologs of yeast ATG6 function in autophagy and are implicated in powdery mildew immunity. Bmc Plant Biol. 2015, 15. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wei, Y.X.; Liu, W.; Hu, W.; Liu, G.Y.; Wu, C.J.; Liu, W.; Zeng, H.Q.; He, C.Z.; Shi, H.T. 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. 2017, 36, 1237–1250. [Google Scholar] [CrossRef]
- Dagdas, Y.F.; Pandey, P.; Tumtas, Y.; Sanguankiattichai, N.; Belhaj, K.; Duggan, C.; Leary, A.Y.; Segretin, M.E.; Contreras, M.P.; Savage, Z.; et al. Host autophagy machinery is diverted to the pathogen interface to mediate focal defense responses against the Irish potato famine pathogen. Elife 2018, 7. [Google Scholar] [CrossRef]
- Dagdas, Y.F.; Belhaj, K.; Maqbool, A.; Chaparro-Garcia, A.; Pandey, P.; Petre, B.; Tabassum, N.; Cruz-Mireles, N.; Hughes, R.K.; Sklenar, J.; et al. An effector of the Irish potato famine pathogen antagonizes a host autophagy cargo receptor. Elife 2016, 5. [Google Scholar] [CrossRef]
- Ustun, S.; Hafren, A.; Liu, Q.S.; Marshall, R.S.; Minina, E.A.; Bozhkov, P.V.; Vierstra, R.D.; Hofius, D. Bacteria Exploit Autophagy for Proteasome Degradation and Enhanced Virulence in Plants. Plant Cell 2018, 30, 668–685. [Google Scholar] [CrossRef] [Green Version]
- Hofius, D.; Schultz-Larsen, T.; Joensen, J.; Tsitsigiannis, D.I.; Petersen, N.H.T.; Mattsson, O.; Jorgensen, L.B.; Jones, J.D.G.; Mundy, J.; Petersen, M. Autophagic Components Contribute to Hypersensitive Cell Death in Arabidopsis. Cell 2009, 137, 773–783. [Google Scholar] [CrossRef] [Green Version]
- Patel, S.; Dinesh-Kumar, S.P. Arabidopsis ATG6 is required to limit the pathogen-associated cell death response. Autophagy 2008, 4, 20–27. [Google Scholar] [CrossRef] [Green Version]
- Hashimi, S.M.; Wu, N.N.; Ran, J.; Liu, J.Z. Silencing Autophagy-Related Gene 2 (ATG2) Results in Accelerated Senescence and Enhanced Immunity in Soybean. Int. J. Mol. Sci. 2021, 22, 11749. [Google Scholar] [CrossRef]
- Wei, Y.X.; Zeng, H.Q.; Liu, W.; Cheng, X.; Zhu, B.B.; Guo, J.R.; Shi, H.T. Autophagy-related genes serve as heat shock protein 90 co-chaperones in disease resistance against cassava bacterial blight. Plant J. 2021, 107, 925–937. [Google Scholar] [CrossRef] [PubMed]
- Yan, Y.; Wang, P.; He, C.Z.; Shi, H.T. MeWRKY20 and its interacting and activating autophagy-related protein 8 (MeATG8) regulate plant disease resistance in cassava. Biochem. Bioph. Res. Co. 2017, 494, 20–26. [Google Scholar] [CrossRef] [PubMed]
- Han, S.; Wang, Y.; Zheng, X.; Jia, Q.; Zhao, J.; Bai, F.; Hong, Y.; Liu, Y. Cytoplastic Glyceraldehyde-3-Phosphate Dehydrogenases Interact with ATG3 to Negatively Regulate Autophagy and Immunity in Nicotiana benthamiana. Plant Cell 2015, 27, 1316–1331. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Henry, E.; Fung, N.; Liu, J.; Drakakaki, G.; Coaker, G. Beyond glycolysis: GAPDHs are multi-functional enzymes involved in regulation of ROS, autophagy, and plant immune responses. PLoS Genet. 2015, 11, e1005199. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zeng, H.Q.; Xie, Y.W.; Liu, G.Y.; Lin, D.Z.; He, C.Z.; Shi, H.T. Molecular identification of GAPDHs in cassava highlights the antagonism of MeGAPCs and MeATG8s in plant disease resistance against cassava bacterial blight. Plant Mol. Biol. 2018, 97, 201–214. [Google Scholar] [CrossRef] [PubMed]
- Rigault, M.; Citerne, S.; Masclaux-Daubresse, C.; Dellagi, A. Salicylic acid is a key player of Arabidopsis autophagy mutant susceptibility to the necrotrophic bacterium Dickeya dadantii. Sci Rep-Uk 2021, 11. [Google Scholar] [CrossRef]
- Thanthrige, N.; Das Bhowmik, S.; Ferguson, B.J.; Kabbage, M.; Mundree, S.G.; Williams, B. Potential Biotechnological Applications of Autophagy for Agriculture. Front. Plant Sci. 2021, 12. [Google Scholar] [CrossRef]
- Wang, P.; Sun, X.; Wang, N.; Jia, X.; Ma, F.W. Ectopic expression of an autophagy-associated MdATG7b gene from apple alters growth and tolerance to nutrient stress in Arabidopsis thaliana. Plant Cell Tiss. Org. 2017, 128, 9–23. [Google Scholar] [CrossRef]
- Wang, Y.; Cao, J.J.; Wang, K.X.; Xia, X.J.; Shi, K.; Zhou, Y.H.; Yu, J.Q.; Zhou, J. BZR1 Mediates Brassinosteroid-Induced Autophagy and Nitrogen Starvation in Tomato. Plant Physiol. 2019, 179, 671–685. [Google Scholar] [CrossRef] [Green Version]
- Wang, P.; Nolan, T.M.; Yin, Y.H.; Bassham, D.C. Identification of transcription factors that regulate ATG8 expression and autophagy in Arabidopsis. Autophagy 2020, 16, 123–139. [Google Scholar] [CrossRef]
- Bao, Y.; Song, W.M.; Wang, P.; Yu, X.; Li, B.; Jiang, C.; Shiu, S.H.; Zhang, H.; Bassham, D.C. COST1 regulates autophagy to control plant drought tolerance. Proc. Natl. Acad. Sci. USA 2020, 117, 7482–7493. [Google Scholar] [CrossRef] [PubMed]
- Yang, C.; Shen, W.; Yang, L.; Sun, Y.; Li, X.; Lai, M.; Wei, J.; Wang, C.; Xu, Y.; Li, F.; et al. HY5-HDA9 Module Transcriptionally Regulates Plant Autophagy in Response to Light-to-Dark Conversion and Nitrogen Starvation. Mol. Plant 2020, 13, 515–531. [Google Scholar] [CrossRef] [PubMed]
- Avin-Wittenberg, T.; Baluska, F.; Bozhkov, P.V.; Elander, P.H.; Fernie, A.R.; Galili, G.; Hassan, A.; Hofius, D.; Isono, E.; Le Bars, R.; et al. Autophagy-related approaches for improving nutrient use efficiency and crop yield protection. J. Exp. Bot. 2018, 69, 1335–1353. [Google Scholar] [CrossRef] [PubMed]
Genes | Plant Species | Genetic Manipulation a | Phenotypes | Ref |
---|---|---|---|---|
GmATG8c | Soybean | OE | Improved tolerance to N starvation in soybean calli and Arabidopsis OE lines | [32] |
SiATG8a | Foxtail millet | OE | Conferring enhanced tolerance to N starvation in Arabidopsis and rice OE lines; improved tolerance to drought stress in Arabidopsis OE lines | [33,45] |
MdATG8i | Apple | OE | Enhanced vegetative growth, leaf senescence and tolerance to N and C starvation in Arabidopsis OE lines; better tolerance to N/C starvation in apple OE calli; enhanced tolerance to salt and drought in apple OE lines | [40,103,104] |
MdATG3a, MdATG3b | Apple | OE | Arabidopsis OE lines show accelerated growth and bolting, and improved tolerance to mannitol, NaCl, N, and C starvation; apple calli overexpressing MdATG3b improve tolerance to N and C starvation | [46] |
MdATG7b | Apple | OE | Arabidopsis OE lines show accelerated growth and bolting, and improved tolerance to stresses caused by NaCl and N/C starvation | [138] |
MdATG18a | Apple | OE | enhanced tolerance to drought stress and N depletion in the apple OE lines; enhanced tolerance to drought stress in the tomato OE lines | [48,90] |
MdATG9 | Apple | OE | Transgenic apple calli confer enhanced tolerance to N depletion; Arabidopsis OE lines alleviates the negative effects of N deprivation on the root growth | [47] |
OsATG8a | Rice | OE | Increased numbers of tillers and reduced height; increased panicle numbers and yield; improved nitrogen use efficiency (NRE) under normal conditions | [49] |
OsATG8c | Rice | OE | Increased yield under normal conditions; improved NRE under normal or N-deficient conditions | [50] |
OsATG8b | Rice | OE | conferring higher N-recycling efficiency to grains; increased yield under normal conditions | [51] |
ATG5, ATG7 | Arabidopsis | OE | Increased resistance to necrotrophic pathogens and oxidative stress, delayed aging and enhanced growth, seed set, and seed oil content | [79] |
ASMT | Tomato | OE | Enhanced autophagy and thermotolerance | [99] |
BZR1 | Tomato | OE | Enhanced autophagy and tolerance to chilling stress and N starvation | [84,139] |
HsfA1 | Tomato | OE | Enhanced autophagy and tolerance to drought stress | [89] |
AOX | Tomato | OE | Enhanced autophagosome formation and ethylene-mediated drought tolerance | [101] |
MtCAS31 | Medicago truncatula | OE | Improving drought tolerance by mediating selective autophagic degradation of the aquaporin MtPIP2;7 | [102] |
TGA9 | Arabidopsis | OE | Increased autophagy under sucrose starvation and osmotic stress; enhanced tolerance to C starvation | [140] |
COST1 | Arabidopsis | KO | Increased drought tolerance but decreased growth | [141] |
GAPCs | Nicotiana benthamiana | VIGS | Enhanced resistance to the incompatible pathogens tobacco mosaic virus and Pst, as well as compatible pathogen Pseudomonas syringae pv tabaci | [133] |
GAPC1, GAPA1 | Arabidopsis | KO | Enhanced resistance to both the virulent Pst and avirulent Pst expressing the effector AvrRpt2 | [134] |
MeGAPCs | Cassava | VIGS | to Xanthomonas axonopodis pv manihotis (Xam) | [135] |
HY5 | Arabidopsis | KO | Enhanced autophagy and improved tolerance to N/C starvation | [142] |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Wang, J.; Miao, S.; Liu, Y.; Wang, Y. Linking Autophagy to Potential Agronomic Trait Improvement in Crops. Int. J. Mol. Sci. 2022, 23, 4793. https://doi.org/10.3390/ijms23094793
Wang J, Miao S, Liu Y, Wang Y. Linking Autophagy to Potential Agronomic Trait Improvement in Crops. International Journal of Molecular Sciences. 2022; 23(9):4793. https://doi.org/10.3390/ijms23094793
Chicago/Turabian StyleWang, Jingran, Shulei Miao, Yule Liu, and Yan Wang. 2022. "Linking Autophagy to Potential Agronomic Trait Improvement in Crops" International Journal of Molecular Sciences 23, no. 9: 4793. https://doi.org/10.3390/ijms23094793