COST1 regulates autophagy to control plant drought tolerance
Abstract
Plants balance their competing requirements for growth and stress tolerance via a sophisticated regulatory circuitry that controls responses to the external environments. We have identified a plant-specific gene, COST1 (constitutively stressed 1), that is required for normal plant growth but negatively regulates drought resistance by influencing the autophagy pathway. An Arabidopsis thaliana cost1 mutant has decreased growth and increased drought tolerance, together with constitutive autophagy and increased expression of drought-response genes, while overexpression of COST1 confers drought hypersensitivity and reduced autophagy. The COST1 protein is degraded upon plant dehydration, and this degradation is reduced upon treatment with inhibitors of the 26S proteasome or autophagy pathways. The drought resistance of a cost1 mutant is dependent on an active autophagy pathway, but independent of other known drought signaling pathways, indicating that COST1 acts through regulation of autophagy. In addition, COST1 colocalizes to autophagosomes with the autophagosome marker ATG8e and the autophagy adaptor NBR1, and affects the level of ATG8e protein through physical interaction with ATG8e, indicating a pivotal role in direct regulation of autophagy. We propose a model in which COST1 represses autophagy under optimal conditions, thus allowing plant growth. Under drought, COST1 is degraded, enabling activation of autophagy and suppression ofmore »
- Authors:
-
- Iowa State Univ., Ames, IA (United States); Chinese Academy of Sciences, Shanghai (China); Michigan State Univ., East Lansing, MI (United States)
- Chinese Academy of Sciences, Shanghai (China); Ludong Univ., Yantai (China)
- Michigan State Univ., East Lansing, MI (United States)
- Chinese Academy of Sciences, Shanghai (China)
- Ludong Univ., Yantai (China)
- Iowa State Univ., Ames, IA (United States)
- Publication Date:
- Research Org.:
- Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1637442
- Grant/Contract Number:
- SC0018409
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Proceedings of the National Academy of Sciences of the United States of America
- Additional Journal Information:
- Journal Volume: 117; Journal Issue: 13; Journal ID: ISSN 0027-8424
- Publisher:
- National Academy of Sciences
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; autophagy; drought; Arabidopsis; COST1
Citation Formats
Bao, Yan, Song, Wei-Meng, Wang, Peipei, Yu, Xiang, Li, Bei, Jiang, Chunmei, Shiu, Shin-Han, Zhang, Hongxia, and Bassham, Diane C. COST1 regulates autophagy to control plant drought tolerance. United States: N. p., 2020.
Web. doi:10.1073/pnas.1918539117.
Bao, Yan, Song, Wei-Meng, Wang, Peipei, Yu, Xiang, Li, Bei, Jiang, Chunmei, Shiu, Shin-Han, Zhang, Hongxia, & Bassham, Diane C. COST1 regulates autophagy to control plant drought tolerance. United States. https://doi.org/10.1073/pnas.1918539117
Bao, Yan, Song, Wei-Meng, Wang, Peipei, Yu, Xiang, Li, Bei, Jiang, Chunmei, Shiu, Shin-Han, Zhang, Hongxia, and Bassham, Diane C. Fri .
"COST1 regulates autophagy to control plant drought tolerance". United States. https://doi.org/10.1073/pnas.1918539117. https://www.osti.gov/servlets/purl/1637442.
@article{osti_1637442,
title = {COST1 regulates autophagy to control plant drought tolerance},
author = {Bao, Yan and Song, Wei-Meng and Wang, Peipei and Yu, Xiang and Li, Bei and Jiang, Chunmei and Shiu, Shin-Han and Zhang, Hongxia and Bassham, Diane C.},
abstractNote = {Plants balance their competing requirements for growth and stress tolerance via a sophisticated regulatory circuitry that controls responses to the external environments. We have identified a plant-specific gene, COST1 (constitutively stressed 1), that is required for normal plant growth but negatively regulates drought resistance by influencing the autophagy pathway. An Arabidopsis thaliana cost1 mutant has decreased growth and increased drought tolerance, together with constitutive autophagy and increased expression of drought-response genes, while overexpression of COST1 confers drought hypersensitivity and reduced autophagy. The COST1 protein is degraded upon plant dehydration, and this degradation is reduced upon treatment with inhibitors of the 26S proteasome or autophagy pathways. The drought resistance of a cost1 mutant is dependent on an active autophagy pathway, but independent of other known drought signaling pathways, indicating that COST1 acts through regulation of autophagy. In addition, COST1 colocalizes to autophagosomes with the autophagosome marker ATG8e and the autophagy adaptor NBR1, and affects the level of ATG8e protein through physical interaction with ATG8e, indicating a pivotal role in direct regulation of autophagy. We propose a model in which COST1 represses autophagy under optimal conditions, thus allowing plant growth. Under drought, COST1 is degraded, enabling activation of autophagy and suppression of growth to enhance drought tolerance. Our research places COST1 as an important regulator controlling the balance between growth and stress responses via the direct regulation of autophagy.},
doi = {10.1073/pnas.1918539117},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 13,
volume = 117,
place = {United States},
year = {2020},
month = {3}
}
Web of Science
Works referenced in this record:
TOR Is a Negative Regulator of Autophagy in Arabidopsis thaliana
journal, July 2010
- Liu, Yimo; Bassham, Diane C.
- PLoS ONE, Vol. 5, Issue 7
News on ABA transport, protein degradation, and ABFs/WRKYs in ABA signaling
journal, October 2011
- Antoni, Regina; Rodriguez, Lesia; Gonzalez-Guzman, Miguel
- Current Opinion in Plant Biology, Vol. 14, Issue 5
The ATG1/ATG13 Protein Kinase Complex Is Both a Regulator and a Target of Autophagic Recycling in Arabidopsis
journal, October 2011
- Suttangkakul, Anongpat; Li, Faqiang; Chung, Taijoon
- The Plant Cell, Vol. 23, Issue 10
Genetic Engineering for Modern Agriculture: Challenges and Perspectives
journal, June 2010
- Mittler, Ron; Blumwald, Eduardo
- Annual Review of Plant Biology, Vol. 61, Issue 1
Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinase-phosphatase pair
journal, December 2009
- Geiger, Dietmar; Scherzer, Sönke; Mumm, Patrick
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 50
Overexpression of the NDR1/HIN1-Like Gene NHL6 Modifies Seed Germination in Response to Abscisic Acid and Abiotic Stresses in Arabidopsis
journal, February 2016
- Bao, Yan; Song, Wei-Meng; Pan, Jing
- PLOS ONE, Vol. 11, Issue 2
Abscisic Acid Inhibits Type 2C Protein Phosphatases via the PYR/PYL Family of START Proteins
journal, April 2009
- Park, S. -Y.; Fung, P.; Nishimura, N.
- Science
New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0
journal, March 2010
- Guindon, Stéphane; Dufayard, Jean-François; Lefort, Vincent
- Systematic Biology, Vol. 59, Issue 3
Endocytic and autophagic pathways crosstalk in plants
journal, December 2015
- Zhuang, Xiaohong; Cui, Yong; Gao, Caiji
- Current Opinion in Plant Biology, Vol. 28
Arabidopsis OST1 Protein Kinase Mediates the Regulation of Stomatal Aperture by Abscisic Acid and Acts Upstream of Reactive Oxygen Species Production
journal, November 2002
- Mustilli, Anna-Chiara; Merlot, Sylvain; Vavasseur, Alain
- The Plant Cell, Vol. 14, Issue 12
The Unfolded Protein Response Supports Plant Development and Defense as well as Responses to Abiotic Stress
journal, March 2017
- Bao, Yan; Howell, Stephen H.
- Frontiers in Plant Science, Vol. 8
Autophagy: The Master of Bulk and Selective Recycling
journal, April 2018
- Marshall, Richard S.; Vierstra, Richard D.
- Annual Review of Plant Biology, Vol. 69, Issue 1
Calcium channels activated by hydrogen peroxide mediate abscisic acidsignalling in guard cells
journal, August 2000
- Pei, Zhen-Ming; Murata, Yoshiyuki; Benning, Gregor
- Nature, Vol. 406, Issue 6797
Non-26S Proteasome Endomembrane Trafficking Pathways in ABA Signaling
journal, November 2017
- Yu, Feifei; Xie, Qi
- Trends in Plant Science, Vol. 22, Issue 11
The Blue Revolution, Drop by Drop, Gene by Gene
journal, April 2008
- Pennisi, E.
- Science, Vol. 320, Issue 5873
Abscisic Acid: Emergence of a Core Signaling Network
journal, June 2010
- Cutler, Sean R.; Rodriguez, Pedro L.; Finkelstein, Ruth R.
- Annual Review of Plant Biology, Vol. 61, Issue 1
Convergent gene loss following gene and genome duplications creates single-copy families in flowering plants
journal, February 2013
- De Smet, R.; Adams, K. L.; Vandepoele, K.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 8
Selective autophagy mediated by autophagic adapter proteins
journal, March 2011
- Johansen, Terje; Lamark, Trond
- Autophagy, Vol. 7, Issue 3
DEXH Box RNA Helicase–Mediated Mitochondrial Reactive Oxygen Species Production in Arabidopsis Mediates Crosstalk between Abscisic Acid and Auxin Signaling
journal, May 2012
- He, Junna; Duan, Ying; Hua, Deping
- The Plant Cell, Vol. 24, Issue 5
Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis
journal, September 2009
- Umezawa, T.; Sugiyama, N.; Mizoguchi, M.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 41
Guard Cell Inward K + Channel Activity in Arabidopsis Involves Expression of the Twin Channel Subunits KAT1 and KAT2
journal, October 2000
- Pilot, Guillaume; Lacombe, Benoı̂t; Gaymard, Frédéric
- Journal of Biological Chemistry, Vol. 276, Issue 5
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs
journal, September 1997
- Altschul, Stephen F.; Madden, Thomas L.; Schäffer, Alejandro A.
- Nucleic Acids Research, Vol. 25, Issue 17, p. 3389-3402
Role of Arabidopsis NHL family in ABA and stress response
journal, April 2016
- Bao, Yan; Song, Wei-Meng; Zhang, Hong-Xia
- Plant Signaling & Behavior, Vol. 11, Issue 5
Abscisic acid Biosynthesis and Catabolism
journal, June 2005
- Nambara, Eiji; Marion-Poll, Annie
- Annual Review of Plant Biology, Vol. 56, Issue 1
iLIR: A web resource for prediction of Atg8-family interacting proteins
journal, February 2014
- Kalvari, Ioanna; Tsompanis, Stelios; Mulakkal, Nitha C.
- Autophagy, Vol. 10, Issue 5
National Science Foundation-Sponsored Workshop Report: “The 2010 Project”Functional Genomics and the Virtual Plant. A Blueprint for Understanding How Plants Are Built and How to Improve Them
journal, June 2000
- Chory, Joanne; Ecker, Joseph R.; Briggs, Steve
- Plant Physiology, Vol. 123, Issue 2
S ALT AND D ROUGHT S TRESS S IGNAL T RANSDUCTION IN P LANTS
journal, June 2002
- Zhu, Jian-Kang
- Annual Review of Plant Biology, Vol. 53, Issue 1
The Cullin-RING Ubiquitin-Protein Ligases
journal, June 2011
- Hua, Zhihua; Vierstra, Richard D.
- Annual Review of Plant Biology, Vol. 62, Issue 1
Arabidopsis ABA response gene ABI1: features of a calcium-modulated protein phosphatase
journal, June 1994
- Leung, J.; Bouvier-Durand, M.; Morris, P.
- Science, Vol. 264, Issue 5164
Autophagy in Plants – What's New on the Menu?
journal, February 2016
- Michaeli, Simon; Galili, Gad; Genschik, Pascal
- Trends in Plant Science, Vol. 21, Issue 2
Plant NBR1 is a selective autophagy substrate and a functional hybrid of the mammalian autophagic adapters NBR1 and p62/SQSTM1
journal, September 2011
- Svenning, Steingrim; Lamark, Trond; Krause, Kirsten
- Autophagy, Vol. 7, Issue 9
ATG8-Binding UIM Proteins Define a New Class of Autophagy Adaptors and Receptors
journal, April 2019
- Marshall, Richard S.; Hua, Zhihua; Mali, Sujina
- Cell, Vol. 177, Issue 3
Characterization of Arabidopsis Tubby-like proteins and redundant function of AtTLP3 and AtTLP9 in plant response to ABA and osmotic stress
journal, August 2014
- Bao, Yan; Song, Wei-Meng; Jin, Yan-Li
- Plant Molecular Biology, Vol. 86, Issue 4-5
SDIR1 Is a RING Finger E3 Ligase That Positively Regulates Stress-Responsive Abscisic Acid Signaling in Arabidopsis
journal, June 2007
- Zhang, Yiyue; Yang, Chengwei; Li, Yin
- The Plant Cell, Vol. 19, Issue 6
A scaling normalization method for differential expression analysis of RNA-seq data
journal, March 2010
- Robinson, Mark D.; Oshlack, Alicia
- Genome Biology, Vol. 11, Issue 3, Article No. R25
The ubiquitin–26S proteasome system at the nexus of plant biology
journal, May 2009
- Vierstra, Richard D.
- Nature Reviews Molecular Cell Biology, Vol. 10, Issue 6
Autophagy and its role in plant abiotic stress management: The Role of Autophagy in Abiotic Stress
journal, August 2018
- Avin-Wittenberg, Tamar
- Plant, Cell & Environment, Vol. 42, Issue 3
In vitro reconstitution of an abscisic acid signalling pathway
journal, November 2009
- Fujii, Hiroaki; Chinnusamy, Viswanathan; Rodrigues, Americo
- Nature, Vol. 462, Issue 7273
Phosphorylation of the Arabidopsis AtrbohF NADPH oxidase by OST1 protein kinase
journal, August 2009
- Sirichandra, Caroline; Gu, Dan; Hu, Heng-Cheng
- FEBS Letters, Vol. 583, Issue 18
The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools
journal, December 2011
- Lamesch, Philippe; Berardini, Tanya Z.; Li, Donghui
- Nucleic Acids Research, Vol. 40, Issue D1
ATG8 lipidation and ATG8-mediated autophagy in Arabidopsis require ATG12 expressed from the differentially controlled ATG12A AND ATG12B loci: Arabidopsis autophagy requires ATG12
journal, February 2010
- Chung, Taijoon; Phillips, Allison R.; Vierstra, Richard D.
- The Plant Journal, Vol. 62, Issue 3
NBR1-Mediated Selective Autophagy Targets Insoluble Ubiquitinated Protein Aggregates in Plant Stress Responses
journal, January 2013
- Zhou, Jie; Wang, Jian; Cheng, Yuan
- PLoS Genetics, Vol. 9, Issue 1
Activated Expression of an Arabidopsis HD-START Protein Confers Drought Tolerance with Improved Root System and Reduced Stomatal Density
journal, April 2008
- Yu, Hong; Chen, Xi; Hong, Yuan-Yuan
- The Plant Cell, Vol. 20, Issue 4
Overexpression of Arabidopsis Acyl-CoA Binding Protein ACBP3 Promotes Starvation-Induced and Age-Dependent Leaf Senescence
journal, May 2010
- Xiao, Shi; Gao, Wei; Chen, Qin-Fang
- The Plant Cell, Vol. 22, Issue 5
Evolution of gene duplication in plants
journal, June 2016
- Panchy, Nicholas; Lehti-Shiu, Melissa D.; Shiu, Shin-Han
- Plant Physiology
Abiotic stress tolerance mediated by protein ubiquitination
journal, October 2011
- Lyzenga, W. J.; Stone, S. L.
- Journal of Experimental Botany, Vol. 63, Issue 2
Abscisic Acid Activation of Plasma Membrane Ca 2+ Channels in Guard Cells Requires Cytosolic NAD(P)H and Is Differentially Disrupted Upstream and Downstream of Reactive Oxygen Species Production in abi1-1 and abi2-1 Protein Phosphatase 2C Mutants
journal, November 2001
- Murata, Yoshiyuki; Pei, Zhen-Ming; Mori, Izumi C.
- The Plant Cell, Vol. 13, Issue 11
Guard cell abscisic acid signalling and engineering drought hardiness in plants
journal, March 2001
- Schroeder, Julian I.; Kwak, June M.; Allen, Gethyn J.
- Nature, Vol. 410, Issue 6826
Adjusting batch effects in microarray expression data using empirical Bayes methods
journal, April 2006
- Johnson, W. Evan; Li, Cheng; Rabinovic, Ariel
- Biostatistics, Vol. 8, Issue 1
Regulation of Abscisic Acid Biosynthesis
journal, September 2003
- Xiong, Liming; Zhu, Jian-Kang
- Plant Physiology, Vol. 133, Issue 1
The Pfam protein families database: towards a more sustainable future
journal, December 2015
- Finn, Robert D.; Coggill, Penelope; Eberhardt, Ruth Y.
- Nucleic Acids Research, Vol. 44, Issue D1
Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis
journal, June 2007
- Yoo, Sang-Dong; Cho, Young-Hee; Sheen, Jen
- Nature Protocols, Vol. 2, Issue 7
A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants: Fluorescent organelle markers
journal, August 2007
- Nelson, Brook K.; Cai, Xue; Nebenführ, Andreas
- The Plant Journal, Vol. 51, Issue 6
Autophagic Nutrient Recycling in Arabidopsis Directed by the ATG8 and ATG12 Conjugation Pathways
journal, July 2005
- Thompson, Allison R.; Doelling, Jed H.; Suttangkakul, Anongpat
- Plant Physiology, Vol. 138, Issue 4
The transcriptional regulatory network in the drought response and its crosstalk in abiotic stress responses including drought, cold, and heat
journal, May 2014
- Nakashima, Kazuo; Yamaguchi-Shinozaki, Kazuko; Shinozaki, Kazuo
- Frontiers in Plant Science, Vol. 5
The tumor necrosis factor receptor-associated factor (TRAF)-like family protein SEVEN IN ABSENTIA 2 (SINA2) promotes drought tolerance in an ABA-dependent manner in Arabidopsis
journal, December 2013
- Bao, Yan; Wang, Cuiting; Jiang, Chunmei
- New Phytologist, Vol. 202, Issue 1
Linking genes of unknown function with abiotic stress responses by high-throughput phenotype screening
journal, March 2013
- Luhua, Song; Hegie, Alicia; Suzuki, Nobuhiro
- Physiologia Plantarum, Vol. 148, Issue 3
The role of ubiquitin and the 26S proteasome in plant abiotic stress signaling
journal, April 2014
- Stone, Sophia L.
- Frontiers in Plant Science, Vol. 5
A Plasma Membrane Receptor Kinase, GHR1, Mediates Abscisic Acid- and Hydrogen Peroxide-Regulated Stomatal Movement in Arabidopsis
journal, June 2012
- Hua, Deping; Wang, Cun; He, Junna
- The Plant Cell, Vol. 24, Issue 6
NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis
journal, June 2003
- Kwak, J. M.
- The EMBO Journal, Vol. 22, Issue 11
Regulators of PP2C Phosphatase Activity Function as Abscisic Acid Sensors
journal, April 2009
- Ma, Y.; Szostkiewicz, I.; Korte, A.
- Science
Autophagy contributes to regulation of the hypoxia response during submergence in Arabidopsis thaliana
journal, December 2015
- Chen, Liang; Liao, Bin; Qi, Hua
- Autophagy, Vol. 11, Issue 12
MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets
journal, March 2016
- Kumar, Sudhir; Stecher, Glen; Tamura, Koichiro
- Molecular Biology and Evolution, Vol. 33, Issue 7
Degradation of Oxidized Proteins by Autophagy during Oxidative Stress in Arabidopsis
journal, November 2006
- Xiong, Yan; Contento, Anthony L.; Nguyen, Phan Quang
- Plant Physiology, Vol. 143, Issue 1
Rapid, combinatorial analysis of membrane compartments in intact plants with a multicolor marker set
journal, July 2009
- Geldner, Niko; Dénervaud-Tendon, Valérie; Hyman, Derek L.
- The Plant Journal, Vol. 59, Issue 1
Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana
journal, December 1998
- Clough, Steven J.; Bent, Andrew F.
- The Plant Journal, Vol. 16, Issue 6, p. 735-743
The genetic and molecular dissection of abscisic acid biosynthesis and signal transduction in Arabidopsis
journal, January 1998
- Koornneef, Maarten; Léon-Kloosterziel, Karen M.; Schwartz, Steven H.
- Plant Physiology and Biochemistry, Vol. 36, Issue 1-2
Transcriptional Regulatory Networks in Cellular Responses and Tolerance to Dehydration and cold Stresses
journal, June 2006
- Yamaguchi-Shinozaki, Kazuko; Shinozaki, Kazuo
- Annual Review of Plant Biology, Vol. 57, Issue 1
Arabidopsis cargo receptor NBR1 mediates selective autophagy of defective proteins
journal, September 2019
- Jung, Hyera; Lee, Han Nim; Marshall, Richard S.
- Journal of Experimental Botany, Vol. 71, Issue 1
The Plant Cuticle Is Required for Osmotic Stress Regulation of Abscisic Acid Biosynthesis and Osmotic Stress Tolerance in Arabidopsis
journal, May 2011
- Wang, Zhen-Yu; Xiong, Liming; Li, Wenbo
- The Plant Cell, Vol. 23, Issue 5
HMMER web server: interactive sequence similarity searching
journal, May 2011
- Finn, R. D.; Clements, J.; Eddy, S. R.
- Nucleic Acids Research, Vol. 39, Issue suppl
Pfam: the protein families database
journal, November 2013
- Finn, Robert D.; Bateman, Alex; Clements, Jody
- Nucleic Acids Research, Vol. 42, Issue D1
Linking Autophagy to Abiotic and Biotic Stress Responses
journal, May 2019
- Signorelli, Santiago; Tarkowski, Łukasz Paweł; Van den Ende, Wim
- Trends in Plant Science, Vol. 24, Issue 5
Negative Regulation of Anthocyanin Biosynthesis in Arabidopsis by a miR156-Targeted SPL Transcription Factor
journal, April 2011
- Gou, Jin-Ying; Felippes, Felipe F.; Liu, Chang-Jun
- The Plant Cell, Vol. 23, Issue 4
Ubiquitin-Mediated Control of Plant Hormone Signaling
journal, June 2012
- Kelley, Dior R.; Estelle, Mark
- Plant Physiology, Vol. 160, Issue 1
Selective Autophagy: ATG8 Family Proteins, LIR Motifs and Cargo Receptors
journal, January 2020
- Johansen, Terje; Lamark, Trond
- Journal of Molecular Biology, Vol. 432, Issue 1
Autophagy: Pathways for Self-Eating in Plant Cells
journal, June 2012
- Liu, Yimo; Bassham, Diane C.
- Annual Review of Plant Biology, Vol. 63, Issue 1
Autophagy is required for tolerance of drought and salt stress in plants
journal, October 2009
- Liu, Yimo; Xiong, Yan; Bassham, Diane C.
- Autophagy, Vol. 5, Issue 7
Visualization of autophagy in Arabidopsis using the fluorescent dye monodansylcadaverine and a GFP-AtATG8e fusion protein: Visualization of autophagy in Arabidopsis
journal, April 2005
- Contento, Anthony L.; Xiong, Yan; Bassham, Diane C.
- The Plant Journal, Vol. 42, Issue 4
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
journal, December 2014
- Love, Michael I.; Huber, Wolfgang; Anders, Simon
- Genome Biology, Vol. 15, Issue 12
IRE1B degrades RNAs encoding proteins that interfere with the induction of autophagy by ER stress in Arabidopsis thaliana
journal, August 2018
- Bao, Yan; Pu, Yunting; Yu, Xiang
- Autophagy, Vol. 14, Issue 9
A protein kinase-phosphatase pair interacts with an ion channel to regulate ABA signaling in plant guard cells
journal, December 2009
- Lee, Sung Chul; Lan, Wenzhi; Buchanan, Bob B.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 50
Widespread Whole Genome Duplications Contribute to Genome Complexity and Species Diversity in Angiosperms
journal, March 2018
- Ren, Ren; Wang, Haifeng; Guo, Chunce
- Molecular Plant, Vol. 11, Issue 3