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Autophagy is required for tolerance of drought and salt stress in plants
Open accessAbstract
Autophagy is a protein degradation process in which cells recycle cytoplasmic contents when subjected to environmental stress conditions or during certain stages of development. Upon the induction of autophagy, a double membrane autophagosome forms around cytoplasmic components and delivers them to the vacuole or lysosome for degradation. In plants, autophagy has been shown previously to be induced during abiotic stresses including nutrient starvation and oxidative stress. In this paper, we demonstrate the induction of autophagy in high salt and osmotic stress conditions, concomitant with the upregulation of expression of an Arabidopsis thaliana autophagy-related gene AtATG18a. Autophagy-defective RNAi-AtATG18a plants are more sensitive to salt and drought conditions than wild-type plants, demonstrating a role for autophagy in the response to these stresses. NADPH oxidase inhibitors block autophagy induction upon nutrient starvation and salt stress, but not during osmotic stress, indicating that autophagy can be activated by NADPH oxidase-dependent or -independent pathways. Together our results indicate that diverse environmental stresses can induce autophagy and that autophagy is regulated by distinct signaling pathways in different conditions.
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“Autophagy is the major pathway by which proteins and organelles are targeted for degradation in the vacuoles of plants (Liu et al., 2009).”
From Responses of Nannochloropsis oceanica IMET1 to Long-Term Nitrogen Starvation and Recovery (2013) · cites this paper as Liu et al., 2009
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“Plant autophagy is thought to play an important role in nutrient recycling under starvation (Liu et al., 2009).”
From Responses of Nannochloropsis oceanica IMET1 to Long-Term Nitrogen Starvation and Recovery (2013) · cites this paper as Liu et al., 2009
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“Previous reports have indicated that ABA-dependent pathway as well as ABA-independent, but DREB2-dependent pathway was essential in plants drought responses (Liu et al., 2009).”
InfluentialUltrastructure of autophagy in plant cells
van Doorn, W. G., & Papini, A. (2013) · Autophagy · doi:10.4161/auto.26275 · Cited by 151
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New advances in autophagy in plants: Regulation, selectivity and function
Wang, P., Mugume, Y., & Bassham, D. C. (2017) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2017.07.018 · Cited by 150
“Autophagy can be induced by various abiotic stresses, including nutrient starvation, oxidative, salt, drought and heat stress, and autophagy-defective mutants are hypersensitive to these stress conditions [115, 126-130].”
Self-citationSun, X., Jia, X., Huo, L., et al. (2017) · Plant Cell & Environment · doi:10.1111/pce.13110 · Cited by 140
“Arabidopsis ATG18a is required for autophagosome formation during periods of nutrient deprivation, leaf senescence, and abiotic stresses (Liu et al., 2009; Xiong et al., 2005, 2007).”
BackgroundAutophagy in plants: Physiological roles and post‐translational regulation
Qi, H., Xia, F., & Xiao, S. (2020) · Journal of Integrative Plant Biology · doi:10.1111/jipb.12941 · Cited by 144
“In Arabidopsis, AtSINAT1, AtSINAT2, and AtSINAT6 interact with ATG6 (Figure 1) (Lockhart, 2017; Qi et al., 2017).”
Beginning to Understand Autophagy, an Intracellular Self-Degradation System in Plants
Yoshimoto, K. (2012) · Plant and Cell Physiology · doi:10.1093/pcp/pcs099 · Cited by 139
An efficient virus‐induced gene silencing vector for maize functional genomics research
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Hydrogen peroxide mediates spermidine-induced autophagy to alleviate salt stress in cucumber
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Role of plant autophagy in stress response
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“Seven ATG genes (ATG1, ATG2, ATG3, ATG13, ATG16, VPS15, and VPS34) were identified by sequence similarity and have not been functionally described (Hanaoka et al., 2002; Meijer et al., 2007).”
BackgroundSelf-citationPlant Bax Inhibitor-1 interacts with ATG6 to regulate autophagy and programmed cell death
Xu, G., Wang, S., Han, S., Xie, K., Wang, Y., Li, J., & Liu, Y. (2017) · Autophagy · doi:10.1080/15548627.2017.1320633 · Cited by 120
Self-citationTrehalose Accumulation Triggers Autophagy during Plant Desiccation
Williams, B., Njaci, I., Moghaddam, L., Long, H., Dickman, M. B., Zhang, X., & Mundree, S. (2015) · PLOS Genetics · doi:10.1371/journal.pgen.1005705 · Cited by 119
“Notably, autophagy is essential for drought and stress tolerance as autophagy deficient plants are significantly more sensitive to drought [24].”
InfluentialDynamics of Autophagosome Formation
Soto-Burgos, J., Zhuang, X., Jiang, L., & Bassham, D. C. (2017) · PLANT PHYSIOLOGY · doi:10.1104/pp.17.01236 · Cited by 120
“…studied as a response to stress conditions, including nutrient deficiency (Doelling et al., 2002; Hanaoka et al., 2002), salt and drought stress (Liu et al., 2009), heat stress (Zhou et al., 2013; Yang et al., 2016), oxidative stress (Xiong et al., 2007), hypoxia (Chen et al., 2015), pathogen…”
BackgroundSelf-citationGuo, Q., Liu, L., Rupasinghe, T., Roessner, U., & Barkla, B. J. (2022) · PLANT PHYSIOLOGY · doi:10.1093/plphys/kiac123 · Cited by 122
“, 2019), which may be necessary for the rapidly induced endocytosis for nutrient remobilization, and the internalization of PM aquaporin to prevent water loss in plants under salt stress (Liu et al., 2009; Ueda et al., 2016; Luo et al., 2017; Huo et al., 2020).”
BackgroundYang, C., Shen, W., Yang, L., et al. (2020) · Molecular Plant · doi:10.1016/j.molp.2020.02.011 · Cited by 116
Autophagy-related approaches for improving nutrient use efficiency and crop yield protection
Avin‐Wittenberg, T., Baluška, F., Bozhkov, P. V., Elander, P. H., Fernie, A. R., Galili, G., Hassan, A., Hofius, D., Isono, E., Bars, R. L., et al. (2018) · Journal of Experimental Botany · doi:10.1093/jxb/ery069 · Cited by 117
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COST1 regulates autophagy to control plant drought tolerance
Bao, Y., Song, W.-M., Wang, P., Yu, X., Li, B., Jiang, C., Shiu, S., Zhang, H., & Bassham, D. C. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1918539117 · Cited by 112
Self-citationVariations on a theme: plant autophagy in comparison to yeast and mammals
Avin‐Wittenberg, T., Honig, A., & Galili, G. (2011) · PROTOPLASMA · doi:10.1007/s00709-011-0296-z · Cited by 110
“…conditions (Sláviková et al. 2005; Inoue et al. 2006) and was also shown to be involved in the response of plants to various abiotic and biotic stresses as well as in hormonal control (Xiong et al. 2007; Slavikova et al. 2008; Liu et al. 2009; Hayward and Dinesh-Kumar 2010; Vanhee et al. 2011) .”
BackgroundInfluentialNew Insight into the Mechanism and Function of Autophagy in Plant Cells
Yang, X., & Bassham, D. C. (2015) · International review of cytology · doi:10.1016/bs.ircmb.2015.07.005 · Cited by 112
Self-citationLi, Y., Zhang, Y., Wang, L., Wang, P., Xue, Y., Li, X., Qiao, X., Zhang, X., Xu, T., Liu, G., et al. (2017) · Autophagy · doi:10.1080/15548627.2017.1320467 · Cited by 107
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“…responses to abiotic stress conditions, including nutrient deficiency (Hanaoka et al. 2002; Surpin et al. 2003; Yoshimoto et al. 2004; Xiong et al. 2005; Fujiki et al. 2007; Qin et al. 2007), oxidative stress (Xiong et al. 2007a, b) and, most recently, salt and osmotic stress (Liu et al. 2009).”
BackgroundInfluentialRole of autophagy in disease resistance and hypersensitive response-associated cell death
Hofius, D., Munch, D., Bressendorff, S., Mundy, J., & Petersen, M. (2011) · Cell Death and Differentiation · doi:10.1038/cdd.2011.43 · Cited by 104
Zhai, Y., Guo, M., Wang, H., et al. (2016) · Frontiers in Plant Science · doi:10.3389/fpls.2016.00131 · Cited by 102
“The relative expression levels of pepper CaATG genes were calculated following the 2−11CT method (Livak and Schmittgen, 2001), in which the relative expression levels of the control seedlings were set to one and two-fold change was looked as the standard to judge the up- or down-regulation.”
MethodAutophagy in Plants: Both a Puppet and a Puppet Master of Sugars
van Rensburg, H. C. J., den Ende, W. V., & Signorelli, S. (2019) · Frontiers in Plant Science · doi:10.3389/fpls.2019.00014 · Cited by 104
Toward the Storage Metabolome: Profiling the Barley Vacuole
Tohge, T., Ramos, M. S., Nunes‐Nesi, A., Mutwil, M., Giavalisco, P., Steinhauser, D., Schellenberg, M., Willmitzer, L., Persson, S., Martinoia, E., et al. (2011) · PLANT PHYSIOLOGY · doi:10.1104/pp.111.185710 · Cited by 100
“Our current knowledge of the vacuole comes largely from studies of isolated vacuoles as well as cell biological studies of exocytosis, endocytosis, and autophagy (Phan et al., 2008; Liu et al., 2009).”
BackgroundChi, C., Li, X., Fang, P., Xia, X., Shi, K., Zhou, Y., Zhou, J., & Yu, J. (2019) · Journal of Experimental Botany · doi:10.1093/jxb/erz466 · Cited by 102
Seo, D. H., Ahn, M. Y., Park, K. Y., et al. (2016) · The Plant Cell · doi:10.1105/tpc.16.00347 · Cited by 98
Persulfidation of ATG18a regulates autophagy under ER stress in Arabidopsis
Aroca, Á., Yruela, I., Gotor, C., & Bassham, D. C. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2023604118 · Cited by 98
Self-citationCarotenoid deficiency triggers autophagy in the model green algaChlamydomonas reinhardtii
Pérez‐Pérez, M. E., Couso, I., & Crespo, J. L. (2012) · Autophagy · doi:10.4161/auto.18864 · Cited by 96
Mitophagy: A Mechanism for Plant Growth and Survival
Broda, M., Millar, A. H., & Aken, O. V. (2018) · Trends in Plant Science · doi:10.1016/j.tplants.2018.02.010 · Cited by 95
“In normal cellular conditions autophagy may recycle components that accumulate for example oxidative damage [1], but its rate can drastically be increased under a variety of stress conditions, senescence and cell death [2-4].”
BackgroundEvidence for autophagy-dependent pathways of rRNA turnover in Arabidopsis
Floyd, B. E., Morriss, S. C., MacIntosh, G. C., & Bassham, D. C. (2015) · Autophagy · doi:10.1080/15548627.2015.1106664 · Cited by 102
“Carbon-starvation plates were kept in the dark as described.(85,86) T-DNA insertion mutants used in this study were rns2–2 (SALK_069588), atg9–4 (SALK_145980, ABRC stock CS859902), and atg5–1 as described by Thompson et al.”
MethodSelf-citationBao, Y., Pu, Y., Yu, X., Gregory, B. D., Srivastava, R., Howell, S. H., & Bassham, D. C. (2018) · Autophagy · doi:10.1080/15548627.2018.1462426 · Cited by 92
“Autophagy is active at a basal level under normal growth conditions, but is highly upregulated by a wide variety of biotic and abiotic stresses [6-14].”
BackgroundSelf-citationMelatonin enhances the occurrence of autophagy induced by oxidative stress in Arabidopsis seedlings
Wang, P., Sun, X., Wang, N., Tan, D. X., & Ma, F. (2015) · Journal of Pineal Research · doi:10.1111/jpi.12233 · Cited by 92
“Autophagy is also required for plant tolerance to drought conditions and salinity [55], implying that it has a role in removing damaged proteins or organelles during such stressful episodes.”
BackgroundBalfagón, D., Gómez‐Cadenas, ., Rambla, J. L., Granell, A., de Ollas, C., Bassham, D. C., Mittler, R., & Zandalinas, S. I. (2022) · PLANT PHYSIOLOGY · doi:10.1093/plphys/kiac010 · Cited by 96
Self-citationSakuraba, Y., Lee, S., Kim, Y.-S., et al. (2014) · Journal of Experimental Botany · doi:10.1093/jxb/eru008 · Cited by 88
“, 2005), and hypersensitivity to abiotic stresses such as high salinity, oxidative stress, and drought (Xiong et al., 2007; Liu et al., 2009; Zhou et al., 2013).”
BackgroundLi, W., Chen, M., Zhong, L., et al. (2015) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2015.11.035 · Cited by 87
Arabidopsis SINAT Proteins Control Autophagy by Mediating Ubiquitylation and Degradation of ATG13
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“Previous studies have suggested that proteaphagy is induced by long-term MG132 treatment (Marshall et al., 2015).”
BackgroundMethodAbozeid, A., Ying, Z. I., Lin, Y., et al. (2017) · Frontiers in Plant Science · doi:10.3389/fpls.2017.00253 · Cited by 85
“Increasing evidence suggests that diverse abiotic stresses, such as salt, drought, nutrient deficiency and heavy metal toxicity, can induce PCD in plant root tips (Liu et al., 2009; Duan et al., 2010; Xu et al., 2010b; Demidchik et al., 2014).”
BackgroundEffect of Waterlogging-Induced Autophagy on Programmed Cell Death in Arabidopsis Roots
Guan, B., Lin, Z., Liu, D., Li, C., Zhou, Z., Mei, F., Li, J., & Deng, X. (2019) · Frontiers in Plant Science · doi:10.3389/fpls.2019.00468 · Cited by 83
“Previous studies of Arabidopsis thaliana have shown that the expression of genes encoding enzymes related to glucose metabolism, glycolysis, and fermentation increases in response to hypoxia (Liu F. et al., 2005; Loreti et al., 2005; van Dongen et al., 2009).”
BackgroundThe perplexing role of autophagy in plant innate immune responses
Zhou, J., Yu, J., & Chen, Z. (2014) · Molecular Plant Pathology · doi:10.1111/mpp.12118 · Cited by 82
“These studies have shown that autophagy plays an important role in the plant response to nutrient starvation and a spectrum of abiotic stresses, including heat, salt, drought and ROS (Bassham, 2007; Liu et al., 2009, 2012; Xiong et al., 2007a, b; Zhou et al., 2013).”
BackgroundPlant abiotic stress signaling
Akpınar, B. A., Avşar, B., Lucas, S. J., & Budak, H. (2012) · Plant Signaling & Behavior · doi:10.4161/psb.21894 · Cited by 82
Autophagy in crop plants: what's new beyond Arabidopsis ?
Tang, J., & Bassham, D. C. (2018) · Open Biology · doi:10.1098/rsob.180162 · Cited by 81
Self-citationMethods for analysis of autophagy in plants
Bassham, D. C. (2014) · Methods · doi:10.1016/j.ymeth.2014.09.003 · Cited by 78
Self-citationApple autophagy-related protein MdATG3s afford tolerance to multiple abiotic stresses
Wang, P., Sun, X., Jia, X., & Ma, F. (2016) · Plant Science · doi:10.1016/j.plantsci.2016.12.003 · Cited by 81
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“drought tolerance in Arabidopsis [76].”
Unfolded protein response in pollen development and heat stress tolerance
Fragkostefanakis, S., Mesihović, A., Hu, Y., & Schleiff, E. (2016) · Plant Reproduction · doi:10.1007/s00497-016-0276-8 · Cited by 77
Zhou, J., Wang, Z., Wang, X., Li, X., Zhang, Z., Fan, B., Zhu, C., & Chen, Z. (2018) · Autophagy · doi:10.1080/15548627.2017.1422856 · Cited by 78
Arabidopsis NAP1 Regulates the Formation of Autophagosomes
Wang, P., Richardson, C. A., Hawes, C. R., & Hussey, P. J. (2016) · Current Biology · doi:10.1016/j.cub.2016.06.008 · Cited by 76
Drought Drives Spatial Variation in the Millet Root Microbiome
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“A more recent study using autophagy-defective RNAi-AtATG18a plants confirmed that autophagy is essential for tolerance to drought and salt stress in Arabidopsis and loss of function results in increased sensitivity of the AtATG18a mutants to osmotic and salt stress (Liu et al., 2009).”
BackgroundWang, X., Gao, Y., Wang, Q., et al. (2018) · Plant Physiology and Biochemistry · doi:10.1016/j.plaphy.2018.11.026 · Cited by 72
“proteins than wild-type plants due to a lower degradation rate, indicating that autophagy is important in removing oxidized proteins under oxidative and salt stresses (Liu et al., 2009; Xiong et al., 2007).”
BackgroundSaeidi-Sar, S., Abbaspour, H., Afshari, H., & Yaghoobi, S. R. (2012) · Acta Physiologiae Plantarum · doi:10.1007/s11738-012-1107-7 · Cited by 71
“One possibility is that autophagy might be responsible for degrading oxidized proteins under salt stress (Liu et al. 2009).”
BackgroundXu, X., Legay, S., Sergeant, K., Zorzan, S., Leclercq, C. C., Charton, S. A. B., Giarola, V., Liu, X., Challabathula, D., Renaut, J., et al. (2021) · The Plant Journal · doi:10.1111/tpj.15294 · Cited by 70
“These data indicate that the activation of autophagy, denoted as critical in drought responses (Liu et al. , 2009), is involved in the recovery of primary metabolites during the desiccation of C. plantagineum .”
Molecular basis of nitrogen starvation-induced leaf senescence
Sakuraba, Y. (2022) · Frontiers in Plant Science · doi:10.3389/fpls.2022.1013304 · Cited by 70
The roles of autophagy in development and stress responses in Arabidopsis thaliana
Lv, X., Pu, X., Qin, G., Zhu, T., & Lin, H. (2014) · APOPTOSIS · doi:10.1007/s10495-014-0981-4 · Cited by 70
Selamat, N., & Nadarajah, K. K. (2021) · Plants · doi:10.3390/plants10040716 · Cited by 68
Genes for Plant Autophagy: Functions and Interactions
Kim, S.-H., Kwon, C., Lee, J., & Chung, T. (2012) · Molecules and Cells · doi:10.1007/s10059-012-0098-y · Cited by 72
“Cells http://molcells.org stresses (Liu et al., 2009; Shin et al., 2009) in addition to oxidative stress (described above).”
BackgroundAutophagy during drought: function, regulation, and potential application
Tang, J., & Bassham, D. C. (2021) · The Plant Journal · doi:10.1111/tpj.15481 · Cited by 66
Self-citation
Metadata
- Authors
- Liu, Y., Xiong, Y., & Bassham, D. C.
- Affiliations
- Iowa State University (US)
- Corresponding author
- Bassham, Diane C.
- Venue
- Autophagy
- Publisher
- Informa UK Limited
- Published
- 2009-10
- Volume
- 5
- Issue
- 7
- Pages
- 954-963
- ISSN
- 1554-8627 (ISSN-L)
- 1554-8635
- OpenAlex
- W2045981379
- Cited by
- 422
- References
- 0
- Citations by year
- 2026: 19 · 2025: 31 · 2024: 39 · 2023: 25 · 2022: 40 · 2021: 37 · 2020: 43 · 2019: 26 · 2018: 25 · 2017: 37 · 2016: 18 · 2015: 20 · 2014: 16 · 2013: 12 · 2012: 17
- FWCI
- 7.39
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Autophagy (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation (0515998)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Autophagy in Disease and Therapy
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Stress Responses and Tolerance
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
- Keywords
- drought stress, salt stress, osmotic stress, Arabidopsis thaliana, stress tolerance, NADPH oxidase, nutrient deprivation, oxidative stress, stress signaling pathways
- MeSH terms
- Autophagy-Related Proteins, Autophagy, Enzyme Inhibitors, Imidazoles, Mannitol, Osmotic Pressure, Sodium Chloride, Stress, Physiological, Signal Transduction, Arabidopsis, NADPH Oxidases, Arabidopsis Proteins, RNA Interference, Droughts
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