Verslues, Paul E. (韋保羅)

Research Fellow

  • PhD University of California-Riverside
  • BS, MS University of Missouri-Columbia
  • +886-2-2787-1077(Lab)
  • +886-2-2787-1186(Office)
  • paulv@gate.sinica.edu.tw
  • Drought related signaling and metabolism

Drought related signaling and metabolism

Plant drought resistance is a critical issue in agriculture and is of ever greater interest because of the disruptive effects of climate change.  Plants have intricate mechanisms to detect and respond to decreased water availability that occurs during drought.  Both basic research as well as applied research to enhance performance of economically important plants is limited by the fact that we do not know how plants sense a lack of water and initiate molecular mechanisms important for acclimation and continued productivity.  There are also many changes in metabolism that occur during drought stress with accumulation of free proline being one of the most widely observed.  However, the role of proline metabolism, and other metabolic changes, in drought resistance is also not understood.
Long term goals of the Verslues laboratory are to understand still enigmatic drought sensing and signaling mechanisms as well as better understand metabolic changes associated with drought acclimation (particularly proline metabolism) and their regulation.  For the most promising new mechanisms, we also work toward the application of this knowledge to plant improvement.  Our laboratory has expertise in controlled stress treatments and drought physiology as well as methods to apply molecular genetics and cell biology techniques to the study of plant stress.  We also maintain collaborations with quantitative genetics and biochemist with interest in plant stress and metabolism.       

Three synergistic research aims of Verslues laboratory are:

1.Stress function of proline metabolism and its regulation.

We seek to understand how proline metabolism (Figure 1) contributes to drought resistance (Sharma et al., 2011; Bhaskara et al., 2015) and also use proline as a readout of drought sensing and signaling.  Genes found in a forward genetic screen for mutants having altered expression of a Proline Dehydrogenase1 (PDH1promoter:Luciferase reporter (Figure 2), as well as study of the proline synthesis enzyme P5CS1 are revealing how plant metabolism changes and is regulated during drought acclimation.  In particular, several lines of evidence point to an extensive role of proline metabolism in modulating cellular redox status and connection to organelle (chloroplast and mitochondria) metabolism.

Figure 1: Core pathways of proline metabolism.  P5CS1 and ProDH1 (PDH1) are key stress-regulated enzymes in proline synthesis and catabolism, respectively.

Figure 2: Seedling luciferase imaging of a mutant having altered expression of PDH1promoter:Luciferase reporter.  PDH1 expression is normally repressed by stress; however, this mutant maintains high PDH1promoter:Luciferase expression (indicated by the red color) under both control and stress conditions. This mutant , as well as other similar mutants isolated in our screen also has increased proline accumulation under stress.  Mutants with reduced PDH1promoter:Luciferase expression were also isolated in this screen and are being characterized.

2.Drought-related signaling mechanisms.

We have identified a membrane-associated protein AFL1 (Kumar et al. 2015) as well as phosphorylation and cytoskeleton mechanisms as key factors which can promote growth during drought (Figure 3).  Study of AFL1 function as well as additional drought signaling mechanisms identified by phosphoproteomics and the PDH1promoter:Luciferase screen are ongoing (Figure 2).

Figure 3: New cellular mechanisms affecting plant growth during drought.

A.Diagram of proposed AFL1 function at the plasma membrane and endomembrane leading to better growth maintainence during drought.  Diagram is from Kumar et al., 2015).
B.Mutants of previously uncharacterized protein phosphatases have more extensive recovery of microtubule structure during drought acclimation.

3.Natural variation in drought acclimation phenotypes. 

Variation in drought-induced proline accumulation among Arabidopsis accessions identified numerous candidate loci as effectors of proline accumulation and, potentially, drought adaptation (Verslues et al., 2014; Sharma et al., 2013; Kesari et al., 2012) (Figure 4).  Currently we are applying similar methods to stress-induced abscisic acid (ABA) accumulation.

Figure 4:  Differences in P5CS1 intron sequence between Arabidopsis accessions determine the extent of P5CS1 alternative splicing.  This variation is in turn related to differences in proline accumulation and adaptation to environments with different water availability.  Figure is from Kesari et al., 2012.

All publication list

Selected publication list

  • Wong MM, Huang X-J, Bau Y-C, Verslues PE* (2024) AT Hook-Like 10 phosphorylation determines Ribosomal RNA Processing 6-Like 1 (RRP6L1) chromatin association and growth suppression during water stress. Plant Cell & Environment 47: 24-37
  • Eckardt NA, Cutler S, Juenger TE, Marshall-Colon A, Udvardi M, Verslues PE (2023) Focus on climate change and plant abiotic stress biology. Plant Cell 35:1-3
  • Juenger TE*, Verslues PE* (2023) Time for a drought experiment: Do you know your plants’ water status?  Plant Cell 35:10-23
  • Verslues PE*, Bailey-Serres J, Brodersen C, Buckley TN, Conti L, Christmann A, Dinneny JR, Grill E, Hayes S, Heckman RW, Hsu P-K, Juenger TE, Mas P, Munnik T, Nelissen H, Sack L, Schroeder JI, Testerink C, Tyerman SD, Umezawa T, Wigge PA (2023) Burning questions for a warming and changing world: 15 unknowns in plant abiotic stress. Plant Cell 35:67-108
  • Bhaskara GB, Lasky JR, Razzaque S, Zhang L, Haque T, Bonnette JE, Civelek GZ, Verslues PE, Juenger TE* (2022) Natural variation identifies new effectors of water use efficiency in Arabidopsis. Proceedings of the National Academy of Sciences USA  119: (33) e2205305119
  • Verslues PE*, Longkumer T (2022) Size and activity of the root meristem: a key for drought resistance and a key model of drought-related signaling.  Physiologia Plantarum 174: e13622
  • Longkumer T, Chen C-Y, Biancucci M, Bhaskara GB, Verslues PE* (2022) Spatial differences in stoichiometry of EGR phosphatase and Microtubule-Associated Stress Protein 1 control root meristem activity during drought stress.  Plant Cell 34: 742–758
  • GL Chong, MH Foo, WD Lin, MM Wong, PE Verslues* (2019) Highly ABA-Induced 1 (HAI1)-Interacting protein HIN1 and drought acclimation-enhanced splicing efficiency at intron retention sites. Proceedings of the National Academy of Sciences 116(44):22376-22385.
  • GB Bhaskara, MM Wong, PE Verslues* (2019) The flip side of phospho‐signalling: Regulation of protein dephosphorylation and the protein phosphatase 2Cs. Plant, cell & environment 42 (10), 2913-2930
  • Kumar MN, Bau Y-C, Longkumer T, Verslues PE* (2019) Low water potential and At14a-Like1 (AFL1) effects on endocytosis and actin filament organization. Plant Physiology 179: 1594-1607
  • Kalladan R, Lasky JR, Sharma S, Kumar MN, Juenger TE, Des Marais DL, Verslues PE* (2019) Natural variation in 9-cis-epoxycartenoid dioxygenase 3 and ABA accumulation. Plant Physiology 179: 1620-1631
  • Wong MM, Bhaskara GB, Wen T-N, Lin W-D, Nguyen TT, Chong G-L, Verslues PE (2019) Phosphoproteomics of Arabidopsis Highly ABA-Induced1 identifies AT-Hook Like10 phosphorylation required for stress growth regulation. Proceedings of the National Academy of Sciences USA  116 (6): 2354-2363
  • Kalladan R, Lasky JR, Chang TZ, Sharma S, Juenger TE, Verslues PE (2017) Natural variation identifies genes affecting drought-induced Abscisic Acid accumulation in Arabidopsis thaliana. Proceedings of the National Academy of Sciences USA  114: 11536-11541
  • Bhaskara GB, Nguyen TT, Yang T-H, Verslues PE (2017) Analysis of Phosphoproteome Remodeling After Short Term Water Stress and ABA Treatments versus Longer Term Water Stress Acclimation. Frontiers in Plant Science 8: 523
  • Wong MM, Chong GL, Verslues PE (2017) Epigenetics and RNA processing: Connections to drought, salt and ABA?  In: Methods in Molecular Biology, Plant Stress Tolerance: Methods and Protocols (Second Edition) vol 1631, Chapter 1. Sunkar, R ed, Springer
  • Verslues PE (2017) Rapid quantitation of Abscisic Acid by GC-MS/MS for studies of abiotic stress response.  In: Methods in Molecular Biology, Plant Stress Tolerance: Methods and Protocols (Second Edition), vol 1631, Chapter 21. Sunkar, R ed, Springer
  • Bhaskara GB, Wen T-N, Nguyen TT, Verslues PE (2017) Protein Phosphatase 2Cs and Microtubule-Associated Stress Protein 1 control microtubule stability, plant growth, and drought response.  Plant Cell 29: 169-191
  •  Des Marais D*, Juenger TE, Chang, TZ, Verslues PE, Lasky JR (2017) Interactive effects of water limitation and elevated temperature on the physiology, development, and fitness of diverse accessions of Brachypodium distachyon.  New Phytologist  214(1): 132-144
  •  Verslues PE (2017) Time to grow: Factors that control plant growth during mild to moderate drought stress. Plant Cell & Environment  40: 177-179  (commentary article)
  • Shinde S, Villamor JG, Lin W-D, Sharma S, Verslues PE (2016) Proline coordination with fatty acid synthesis and redox metabolism of chloroplast and mitochondria. Plant Physiology 172: 1074-1088.
  • Verslues PE (2016) ABA and cytokinins: challenge and opportunity for plant stress research. Plant Molecular Biology 91:629-640 (review)
  • Kumar MN1, Hsieh Y-F1, Verslues PE (2015) At14a-Like1 participates in membrane associated mechanisms promoting growth during drought in Arabidopsis thaliana.  Proceedings of the National Academy of Sciences USA 112: 10545-10550 (1. Equally contributing authors)
  • Bhaskara GB, Yang T-H, Verslues PE (2015) Dynamic proline metabolism: Importance and regulation in water limited environments. Frontiers in Plant Science6: 484. doi: 410.3389/fpls.2015.00484
  • Lovell JT*, Mullen JL, Lowry DB, Awole K, Richards JH, Sen S, Verslues PE, Juenger TE, McKay JK (2015) Exploiting differential gene expression and epistasis to discover candidate genes for drought-associated QTLs in Arabidopsis thalianaPlant Cell 27: 969-983
  • Haswell ES, Verslues PE (2015) The ongoing search for the molecular basis of plant osmosensing.  Journal of General Physiology 145: 389–394
  • Kumar MN, Verslues PE (2015) Stress physiology functions of Arabidopsis Histidine Kinase (AHK) cytokinin receptors. Physiologia Plantarum 154: 369–380
  • Wilson ME, Basu MR, Bhaskara GB, Verslues PE, Haswell ES (2014) Plastid hypoosmotic stress activates cellular osmotic stress responses.  Plant Physiology 165: 119-128
  • Verslues PE1, Lasky JR1, Juenger TE, Liu T-W, Kumar MN (2014) Genome wide association mapping combined with reverse genetics identifies new effectors of low water potential-induced proline accumulation in Arabidopsis thaliana.  Plant Physiology 164: 144-159       1. Co-first authors
  • Sharma S, Shinde S, Verslues PE  (2013) Functional characterization of an ornithine cyclodeaminase-like protein of Arabidopsis thaliana.  BMC Plant Biology13:182
  • Verslues PE, Bhaskara GB, Kesari R, Kumar MN (2013) Drought tolerance mechanisms and their molecular basis.  In: Plant Abiotic Stress-Second Edition;  Jenks, M.A. and Hasegawa, P.M. eds.; John Wilely and Sons, Inc.  (review book chapter)
  • Kumar MN, Jane W-N, Verslues PE (2013) Role of the putative osmosensor Arabidopsis Histidine Kinase 1 (AHK1) in dehydration avoidance and low water potential response.  Plant Physiology 161: 942-953   (Reccomended by Faculty of 1000)
  • Sharma S., Lin W, Villamor JG, Verslues PE (2013) Divergent low water potential response in Arabidopsis thaliana accessions Landsberg erecta and Shahdara.  Plant Cell & Environment 36: 994-1008
  • Bhaskara GB, Nguyen TT, Verslues PE (2012) Unique drought resistance functions of the Highly-ABA-Induced Clade A protein phosphatase 2Cs.  Plant Physiology 160: 379-395
  • Kesari R, Lasky JR, Villamor JG, Des Marais DL, Chen Y-JC, Liu T-W, Lin W, Juenger TE, Verslues PE (2012) Intron-mediated alternative splicing of Arabidopsis P5CS1 and its association with natural variation in proline and climate adaptation.  Proceedings of the National Academy of Sciences USA 109: 9197-9202
  • Sharma S, Villamor JG, Verslues PE (2011) Essential role of tissue specific proline synthesis and catabolism in growth and redox balance at low water potential.  Plant Physiology 157: 292-304
  • Verslues PE, Juenger TE (2011) Drought, metabolites and Arabidopsis natural variation: a promising combination for understanding adaptation to water-limited environments.  Current Opinion in Plant Biology 14: 240–245
  • Verslues PE, Sharma S (2010) Proline metabolism and its implications for plant-environment interaction.  The Arabidopsis Book 8: 140
  • Sharma S, Verslues PE (2010) Mechanisms independent of abscisic acid (ABA) or proline feedback have a predominant role in transcriptional regulation of proline metabolism during low water potential and stress recovery.  Plant Cell & Environment 33: 1838-1851
  • Verslues PE  (2010) Quantification of water stress-induced osmotic adjustment and proline accumulation for Arabidopsis thaliana molecular genetic studies.  In R. Sunkar ed.  Plant Stress Tolerance, Methods in Molecular Biology 639.  Springer Science+Business Media, LLC. (methods book chapter)
Neha Upadhyay Tiwari
Postdoctoral Fellow
Tai Chien Luong
Research Assistant
Hao-Yi Chang
Research Assistant
Rishima Maheendran
Doctoral Student
Shih-Shan Huang
Lab manager