Coordination and Crosstalk between Autophagosome and Multivesicular Body Pathways in Plant Stress Responses

Bassham, 2006, Autophagy in development and stress responses of plants, Autophagy, 2, 2, 10.4161/auto.2092

Levine, 2011, Autophagy in immunity and inflammation, Nature, 469, 323, 10.1038/nature09782

Wang, 2016, Autophagy: An Important Biological Process That Protects Plants from Stressful Environments, Front. Plant Sci., 7, 2030

Zhuang, 2018, Dynamics of Autophagosome Formation, Plant Physiol., 176, 219, 10.1104/pp.17.01236

Hanson, 2012, Multivesicular body morphogenesis, Annu. Rev. Cell Dev. Biol., 28, 337, 10.1146/annurev-cellbio-092910-154152

Li, 2018, Biogenesis and Function of Multivesicular Bodies in Plant Immunity, Front. Plant Sci., 9, 979, 10.3389/fpls.2018.00979

Goodman, 2016, Endocytosis and Endosomal Trafficking in Plants, Annu. Rev. Plant Biol., 67, 309, 10.1146/annurev-arplant-043015-112242

Bassham, 2007, Plant autophagy—More than a starvation response, Curr. Opin. Plant Biol., 10, 587, 10.1016/j.pbi.2007.06.006

Wang, F., Shang, Y., Fan, B., Yu, J.Q., and Chen, Z. (2014). Arabidopsis LIP5, a positive regulator of multivesicular body biogenesis, is a critical target of pathogen-responsive MAPK cascade in plant basal defense. PLoS Pathog., 10.

Wang, 2015, A Critical Role of Lyst-Interacting Protein5, a Positive Regulator of Multivesicular Body Biogenesis, in Plant Responses to Heat and Salt Stresses, Plant Physiol., 169, 497, 10.1104/pp.15.00518

Lai, 2011, A critical role of autophagy in plant resistance to necrotrophic fungal pathogens, Plant J. Cell Mol. Biol., 66, 953, 10.1111/j.1365-313X.2011.04553.x

Liu, 2009, Autophagy is required for tolerance of drought and salt stress in plants, Autophagy, 5, 954, 10.4161/auto.5.7.9290

Zhou, J., Yu, J.Q., and Chen, Z. (2014). The Perplexing Role of Autophagy in Plant Innate Immune Responses. Mol. Plant Pathol.

Michaeli, 2016, Autophagy in Plants—What’s New on the Menu?, Trends Plant Sci., 21, 134, 10.1016/j.tplants.2015.10.008

Pu, Y., and Bassham, D.C. (2013). Links between ER stress and autophagy in plants. Plant Signal. Behav., 8.

Slavikova, 2005, The autophagy-associated Atg8 gene family operates both under favourable growth conditions and under starvation stresses in Arabidopsis plants, J. Exp. Bot., 56, 2839, 10.1093/jxb/eri276

Wang, 2011, The autophagy gene, ATG18a, plays a negative role in powdery mildew resistance and mildew-induced cell death in Arabidopsis, Plant Signal. Behav., 6, 1408, 10.4161/psb.6.9.16967

Zhou, J., Wang, J., Cheng, Y., Chi, Y.J., Fan, B., Yu, J.Q., and Chen, Z. (2013). NBR1-Mediated Selective Autophagy Targets Insoluble Ubiquitinated Protein Aggregates in Plant Stress Responses. PLoS Genet., 9.

Zhou, J., Zhang, Y., Qi, J., Chi, Y., Fan, B., Yu, J.Q., and Chen, Z. (2014). E3 Ubiquitin Ligase CHIP and NBR1-Mediated Selective Autophagy Protect Additively against Proteotoxicity in Plant Stress Responses. PLoS Genet., 10.

Lenz, 2011, Autophagy differentially controls plant basal immunity to biotrophic and necrotrophic pathogens, Plant J. Cell Mol. Biol., 66, 818, 10.1111/j.1365-313X.2011.04546.x

Liu, 2005, Autophagy regulates programmed cell death during the plant innate immune response, Cell, 121, 567, 10.1016/j.cell.2005.03.007

Seay, 2005, Life after death: Are autophagy genes involved in cell death and survival during plant innate immune responses?, Autophagy, 1, 185, 10.4161/auto.1.3.2080

Ustun, 2018, Bacteria Exploit Autophagy for Proteasome Degradation and Enhanced Virulence in Plants, Plant Cell, 30, 668, 10.1105/tpc.17.00815

Haxim, Y., Ismayil, A., Jia, Q., Wang, Y., Zheng, X., Chen, T., Qian, L., Liu, N., Wang, Y., and Han, S. (2017). Autophagy functions as an antiviral mechanism against geminiviruses in plants. Elife, 6.

Ismayil, A., Yang, M., and Liu, Y. (2019). Role of autophagy during plant-virus interactions. Semin. Cell Dev. Biol.

Dubeaux, 2018, Metal Sensing by the IRT1 Transporter-Receptor Orchestrates Its Own Degradation and Plant Metal Nutrition, Mol. Cell, 69, 953, 10.1016/j.molcel.2018.02.009

Shin, 2013, IRT1 degradation factor1, a ring E3 ubiquitin ligase, regulates the degradation of iron-regulated transporter1 in Arabidopsis, Plant Cell, 25, 3039, 10.1105/tpc.113.115212

Fader, 2006, Multivesicular bodies and autophagy in erythrocyte maturation, Autophagy, 2, 122, 10.4161/auto.2.2.2350

Fader, 2009, Autophagy and multivesicular bodies: Two closely related partners, Cell Death Differ., 16, 70, 10.1038/cdd.2008.168

Muller, 2015, The coordinated action of the MVB pathway and autophagy ensures cell survival during starvation, Elife, 4, e07736, 10.7554/eLife.07736

Shin, 2017, The formation of multivesicular bodies in activated blastocysts is influenced by autophagy and FGF signaling in mice, Sci. Rep., 7, 41986, 10.1038/srep41986

Cui, 2018, The Multivesicular Body and Autophagosome Pathways in Plants, Front. Plant Sci., 9, 1837, 10.3389/fpls.2018.01837

Zhuang, 2015, Endocytic and autophagic pathways crosstalk in plants, Curr Opin Plant Biol., 28, 39, 10.1016/j.pbi.2015.08.010

Mao, 2011, Phosphorylation of a WRKY transcription factor by two pathogen-responsive MAPKs drives phytoalexin biosynthesis in Arabidopsis, Plant Cell, 23, 1639, 10.1105/tpc.111.084996

Liao, C.Y., and Bassham, D.C. (2019). Combating stress: The interplay between hormone signaling and autophagy in plants. J. Exp. Bot.

Signorelli, 2019, Linking Autophagy to Abiotic and Biotic Stress Responses, Trends Plant Sci., 24, 413, 10.1016/j.tplants.2019.02.001

Nagel, 2017, Arabidopsis SH3P2 is an ubiquitin-binding protein that functions together with ESCRT-I and the deubiquitylating enzyme AMSH3, Proc. Natl. Acad. Sci. USA, 114, E7197, 10.1073/pnas.1710866114

Zhuang, 2014, Autophagosome biogenesis in plants: Roles of SH3P2, Autophagy, 10, 704, 10.4161/auto.28060

Zhuang, 2013, A BAR-domain protein SH3P2, which binds to phosphatidylinositol 3-phosphate and ATG8, regulates autophagosome formation in Arabidopsis, Plant Cell, 25, 4596, 10.1105/tpc.113.118307

Gao, 2015, Dual roles of an Arabidopsis ESCRT component FREE1 in regulating vacuolar protein transport and autophagic degradation, Proc. Natl. Acad. Sci. USA, 112, 1886, 10.1073/pnas.1421271112

Cui, 2016, Biogenesis of Plant Prevacuolar Multivesicular Bodies, Mol. Plant, 9, 774, 10.1016/j.molp.2016.01.011

Spitzer, 2009, The ESCRT-related CHMP1A and B proteins mediate multivesicular body sorting of auxin carriers in Arabidopsis and are required for plant development, Plant Cell, 21, 749, 10.1105/tpc.108.064865

Erwig, 2017, Chitin-induced and CHITIN ELICITOR RECEPTOR KINASE1 (CERK1) phosphorylation-dependent endocytosis of Arabidopsis thaliana LYSIN MOTIF-CONTAINING RECEPTOR-LIKE KINASE5 (LYK5), New Phytol., 215, 382, 10.1111/nph.14592

Spallek, T., Beck, M., Ben Khaled, S., Salomon, S., Bourdais, G., Schellmann, S., and Robatzek, S. (2013). ESCRT-I mediates FLS2 endosomal sorting and plant immunity. PLoS Genet., 9.

Kasai, 2014, Analysis of endocytosis and ubiquitination of the BOR1 transporter, Methods Mol. Biol., 1209, 203, 10.1007/978-1-4939-1420-3_16

Cuyas, 2015, ESCRT-III-Associated Protein ALIX Mediates High-Affinity Phosphate Transporter Trafficking to Maintain Phosphate Homeostasis in Arabidopsis, Plant Cell, 27, 2560, 10.1105/tpc.15.00393

Liu, 2017, Nitrogen Limitation Adaptation (NLA) is involved in source-to-sink remobilization of nitrate by mediating the degradation of NRT1.7 in Arabidopsis, New Phytol., 214, 734, 10.1111/nph.14396

Haas, 2007, The Arabidopsis AAA ATPase SKD1 is involved in multivesicular endosome function and interacts with its positive regulator LYST-INTERACTING PROTEIN5, Plant Cell, 19, 1295, 10.1105/tpc.106.049346

Lai, 2011, Arabidopsis sigma factor binding proteins are activators of the WRKY33 transcription factor in plant defense, Plant Cell, 23, 3824, 10.1105/tpc.111.090571

Zheng, 2006, Arabidopsis WRKY33 transcription factor is required for resistance to necrotrophic fungal pathogens, Plant J., 48, 592, 10.1111/j.1365-313X.2006.02901.x

Xu, 2015, Mitogen-activated protein kinase cascades in signaling plant growth and development, Trends Plant Sci., 20, 56, 10.1016/j.tplants.2014.10.001

2004, Knocking on the heaven’s wall: Pathogenesis of and resistance to biotrophic fungi at the cell wall, Curr. Opin. Plant Biol., 7, 377, 10.1016/j.pbi.2004.05.004

An, 2006, Multivesicular compartments proliferate in susceptible and resistant MLA12-barley leaves in response to infection by the biotrophic powdery mildew fungus, New Phytol., 172, 563, 10.1111/j.1469-8137.2006.01844.x

An, 2006, Multivesicular bodies participate in a cell wall-associated defence response in barley leaves attacked by the pathogenic powdery mildew fungus, Cell MicroBiol., 8, 1009, 10.1111/j.1462-5822.2006.00683.x

An, 2007, Do plant cells secrete exosomes derived from multivesicular bodies?, Plant Signal. Behav., 2, 4, 10.4161/psb.2.1.3596

Bohlenius, 2010, The multivesicular body-localized GTPase ARFA1b/1c is important for callose deposition and ROR2 syntaxin-dependent preinvasive basal defense in barley, Plant Cell, 22, 3831, 10.1105/tpc.110.078063

Meyer, 2009, Extracellular transport and integration of plant secretory proteins into pathogen-induced cell wall compartments, Plant J., 57, 986, 10.1111/j.1365-313X.2008.03743.x

Nielsen, 2012, Arabidopsis ARF-GTP exchange factor, GNOM, mediates transport required for innate immunity and focal accumulation of syntaxin PEN1, Proc. Natl. Acad. Sci. USA, 109, 11443, 10.1073/pnas.1117596109

Baldrich, 2019, Plant Extracellular Vesicles Contain Diverse Small RNA Species and Are Enriched in 10- to 17-Nucleotide “Tiny” RNAs, Plant Cell, 31, 315, 10.1105/tpc.18.00872

Rutter, 2017, Extracellular Vesicles Isolated from the Leaf Apoplast Carry Stress-Response Proteins, Plant Physiol., 173, 728, 10.1104/pp.16.01253

Rutter, 2018, Extracellular vesicles as key mediators of plant-microbe interactions, Curr Opin Plant Biol., 44, 16, 10.1016/j.pbi.2018.01.008

Berkey, 2017, Homologues of the RPW8 Resistance Protein Are Localized to the Extrahaustorial Membrane that Is Likely Synthesized De Novo, Plant Physiol., 173, 600, 10.1104/pp.16.01539

Nielsen, 2017, VPS9a Activates the Rab5 GTPase ARA7 to Confer Distinct Pre- and Postinvasive Plant Innate Immunity, Plant Cell, 29, 1927, 10.1105/tpc.16.00859

Bozkurt, 2015, Rerouting of plant late endocytic trafficking toward a pathogen interface, Traffic, 16, 204, 10.1111/tra.12245

Dagdas, Y.F., Pandey, P., Tumtas, Y., Sanguankiattichai, N., Belhaj, K., Duggan, C., Leary, A.Y., Segretin, M.E., Contreras, M.P., and Savage, Z. (2018). Host autophagy machinery is diverted to the pathogen interface to mediate focal defense responses against the Irish potato famine pathogen. Elife, 7.

Dagdas, Y.F., Belhaj, K., Maqbool, A., Chaparro-Garcia, A., Pandey, P., Petre, B., Tabassum, N., Cruz-Mireles, N., Hughes, R.K., and Sklenar, J. (2016). An effector of the Irish potato famine pathogen antagonizes a host autophagy cargo receptor. Elife, 5.

Jones, 2006, The plant immune system, Nature, 444, 323, 10.1038/nature05286

Cui, 2014, Activation of the Rab7 GTPase by the MON1-CCZ1 Complex Is Essential for PVC-to-Vacuole Trafficking and Plant Growth in Arabidopsis, Plant Cell, 26, 2080, 10.1105/tpc.114.123141

Kwon, 2013, The Rab GTPase RabG3b positively regulates autophagy and immunity-associated hypersensitive cell death in Arabidopsis, Plant Physiol., 161, 1722, 10.1104/pp.112.208108

Kwon, 2011, Overexpression of constitutively active Arabidopsis RabG3b promotes xylem development in transgenic poplars, Plant Cell Env., 34, 2212, 10.1111/j.1365-3040.2011.02416.x

Li, 2012, Autophagy: A multifaceted intracellular system for bulk and selective recycling, Trends Plant Sci., 17, 526, 10.1016/j.tplants.2012.05.006

Zhuang, 2019, Chloroplast Degradation: Multiple Routes Into the Vacuole, Front. Plant Sci., 10, 359, 10.3389/fpls.2019.00359

Ishida, 2008, Chloroplasts are partially mobilized to the vacuole by autophagy, Autophagy, 4, 961, 10.4161/auto.6804

Wang, 2013, Autophagy contributes to leaf starch degradation, Plant Cell, 25, 1383, 10.1105/tpc.112.108993

Michaeli, 2014, Arabidopsis ATG8-INTERACTING PROTEIN1 is involved in autophagy-dependent vesicular trafficking of plastid proteins to the vacuole, Plant Cell, 26, 4084, 10.1105/tpc.114.129999

Izumi, 2017, Entire Photodamaged Chloroplasts Are Transported to the Central Vacuole by Autophagy, Plant Cell, 29, 377, 10.1105/tpc.16.00637

Spitzer, 2015, The endosomal protein CHARGED MULTIVESICULAR BODY PROTEIN1 regulates the autophagic turnover of plastids in Arabidopsis, Plant Cell, 27, 391, 10.1105/tpc.114.135939

Chaumont, 2014, Aquaporins: Highly regulated channels controlling plant water relations, Plant Physiol., 164, 1600, 10.1104/pp.113.233791

Ueda, 2016, Salt stress induces internalization of plasma membrane aquaporin into the vacuole in Arabidopsis thaliana, Biochem. Biophys. Res. Commun., 474, 742, 10.1016/j.bbrc.2016.05.028

Hachez, 2014, The Arabidopsis abiotic stress-induced TSPO-related protein reduces cell-surface expression of the aquaporin PIP2;7 through protein-protein interactions and autophagic degradation, Plant Cell, 26, 4974, 10.1105/tpc.114.134080

Zhou, 2014, Role and regulation of autophagy in heat stress responses of tomato plants, Front. Plant Sci., 5, 174, 10.3389/fpls.2014.00174

Harper, 2016, Proteome complexity and the forces that drive proteome imbalance, Nature, 537, 328, 10.1038/nature19947

Wurzer, 2015, Oligomerization of p62 allows for selection of ubiquitinated cargo and isolation membrane during selective autophagy, Elife, 4, e08941, 10.7554/eLife.08941

Jung, H., Lee, H.N., Marshall, R.S., Lomax, A.W., Yoon, M.J., Kim, J., Kim, J.H., Vierstra, R.D., and Chung, T. (2019). NBR1 Mediates Selective Autophagy of Defective Proteins in Arabidopsis. J. Exp. Bot.

Zhou, J., Wang, Z., Wang, X., Li, X., Zhang, Z., Fan, B., Zhu, C., and Chen, Z. (2018). Dicot-specific ATG8-interacting ATI3 proteins interact with conserved UBAC2 proteins and play critical roles in plant stress responses. Autophagy.

Apaja, 2014, Protein homeostasis at the plasma membrane, Physiology, 29, 265, 10.1152/physiol.00058.2013

Scheuring, D., Kunzl, F., Viotti, C., Yan, M.S., Jiang, L., Schellmann, S., Robinson, D.G., and Pimpl, P. (2012). Ubiquitin initiates sorting of Golgi and plasma membrane proteins into the vacuolar degradation pathway. BMC Plant Biol., 12.

Nolan, T., Vukasinovic, N., Liu, D., Russinova, E., and Yin, Y. (2019). Brassinosteroids: Multi-Dimensional Regulators of Plant Growth, Development, and Stress Responses. Plant Cell.

Yu, 2017, Non-26S Proteasome Endomembrane Trafficking Pathways in ABA Signaling, Trends Plant Sci., 22, 976, 10.1016/j.tplants.2017.08.009

Guillaumot, 2009, ABA, porphyrins and plant TSPO-related protein, Plant Signal. Behav., 4, 1087, 10.4161/psb.4.11.9796

Honig, 2012, A New Type of Compartment, Defined by Plant-Specific Atg8-Interacting Proteins, Is Induced upon Exposure of Arabidopsis Plants to Carbon Starvation, Plant Cell, 24, 288, 10.1105/tpc.111.093112

Diaz, 2016, Calcium-dependent oligomerization of CAR proteins at cell membrane modulates ABA signaling, Proc. Natl. Acad. Sci. USA, 113, E396, 10.1073/pnas.1512779113

Rodriguez, 2016, FYVE1/FREE1 Interacts with the PYL4 ABA Receptor and Mediates Its Delivery to the Vacuolar Degradation Pathway, Plant Cell, 28, 2291, 10.1105/tpc.16.00178

Fernandez, M.A., Belda-Palazon, B., Julian, J., Coego, A., Lozano-Juste, J., Inigo, S., Rodriguez, L., Bueso, E., Goossens, A., and Rodriguez, P.L. (2019). RBR-type E3 ligases and the Ub-conjugating enzyme UBC26 regulate ABA receptor levels and signaling. Plant Physiol.

Yu, 2016, ESCRT-I Component VPS23A Affects ABA Signaling by Recognizing ABA Receptors for Endosomal Degradation, Mol. Plant, 9, 1570, 10.1016/j.molp.2016.11.002

Li, 2019, The plant ESCRT component FREE1 shuttles to the nucleus to attenuate abscisic acid signalling, Nat. Plants, 5, 512, 10.1038/s41477-019-0400-5

Raikhel, 2012, Endocytic trafficking towards the vacuole plays a key role in the auxin receptor SCF(TIR)-independent mechanism of lateral root formation in A. thaliana, Mol. Plant, 5, 1195, 10.1093/mp/sss066

Luschnig, 2014, The dynamics of plant plasma membrane proteins: PINs and beyond, Development, 141, 2924, 10.1242/dev.103424

Deb, 2014, 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., 165, 1647, 10.1104/pp.114.244376

Sankaranarayanan, 2015, A proposed role for selective autophagy in regulating auxin-dependent lateral root development under phosphate starvation in Arabidopsis, Plant Signal. Behav., 10, e989749, 10.4161/15592324.2014.989749

Feng, 2015, Down-regulation of BdBRI1, a putative brassinosteroid receptor gene produces a dwarf phenotype with enhanced drought tolerance in Brachypodium distachyon, Plant Sci., 234, 163, 10.1016/j.plantsci.2015.02.015

Nolan, 2017, Selective Autophagy of BES1 Mediated by DSK2 Balances Plant Growth and Survival, Dev. Cell, 41, 33, 10.1016/j.devcel.2017.03.013

Northey, 2016, Farnesylation mediates brassinosteroid biosynthesis to regulate abscisic acid responses, Nat. Plants, 2, 16114, 10.1038/nplants.2016.114

Zhou, 2018, Regulation of Arabidopsis brassinosteroid receptor BRI1 endocytosis and degradation by plant U-box PUB12/PUB13-mediated ubiquitination, Proc. Natl. Acad. Sci. USA, 115, E1906, 10.1073/pnas.1712251115

Zhang, 2016, TOR Signaling Promotes Accumulation of BZR1 to Balance Growth with Carbon Availability in Arabidopsis, Curr. Biol., 26, 1854, 10.1016/j.cub.2016.05.005

Nie, 2013, Silencing of tomato RBOH1 and MPK2 abolishes brassinosteroid-induced H(2)O(2) generation and stress tolerance, Plant Cell Env., 36, 789, 10.1111/pce.12014

Xia, 2009, Reactive oxygen species are involved in brassinosteroid-induced stress tolerance in cucumber, Plant Physiol., 150, 801, 10.1104/pp.109.138230

Xia, 2011, Induction of systemic stress tolerance by brassinosteroid in Cucumis sativus, New Phytol., 191, 706, 10.1111/j.1469-8137.2011.03745.x

Wang, 2019, BZR1 Mediates Brassinosteroid-Induced Autophagy and Nitrogen Starvation in Tomato, Plant Physiol., 179, 671, 10.1104/pp.18.01028