Skip to main content
SpringerLink
Log in

MAP3Kθ1 is Involved in Abscisic Acid Signaling in Drought Tolerance and Seed Germination in Arabidopsis

  • Research Article
  • Published:
Journal of Plant Biology Aims and scope Submit manuscript

Abstract

Mitogen-activated protein kinase cascades play pivotal roles in mediating environmental stress responses and plant development. In this study, a loss-of-function mutant of Arabidopsis, map3kθ1, exhibited wider stomatal openings, reduced root elongation, and increased seed germination rate compared with its wild type under exogenous abscisic acid (ABA) treatment. MAP3Kθ1 encodes a MAP kinase kinase kinase (MAP3K) with unknown function. Two overexpression lines of MAP3Kθ1 exhibited inhibited seed germination and narrowed stomata, which were aggravated by ABA treatment. Upregulation of MAP3Kθ1 also resulted in stronger drought tolerance, whereas map3kθ1 was more sensitive to water deficiency, partially due to differences in the water-holding capacity of leaves. The MAP3Kθ1-overexpressing lines also showed a greater ability to maintain root elongation under exogenous ABA. Expression of MAP3Kθ1 was inhibited by ABA, H2O2, and methyl viologen treatments in roots. The MAP3Kθ1-overexpressing lines accumulated more ABA by promoting its biogenesis and inhibiting its catabolism, whereas the map3kθ1 mutant accumulated less ABA, compared with wild-type plants. These findings indicate that MAP3Kθ1 promotes ABA accumulation to regulate stomatal movement, root elongation, and seed germination, while the ABA–H2O2 signaling module inhibits MAP3Kθ1 expression through feedback regulation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Arve LE, Carvalho DR, Olsen JE, Torre S (2014) ABA induces H2O2 production in guard cells, but does not close the stomata on Vicia faba leaves developed at high air humidity. Plant Signal Behav 9(7):1–9

    Google Scholar 

  • Bauer H, Ache P, Lautner S, Fromm J, Hartung W, Al-Rasheid KA, Sonnewald S, Sonnewald U, Kneitz S, Lachmann N, Mendel RR, Bittner F, Hetherington AM, Hedrich R (2013) The stomatal response to reduced relative humidity requires guard cell-autonomous ABA synthesis. Curr Biol 23(1):53–57

    PubMed  CAS  Google Scholar 

  • Bechtold N (1993) In planta Agrobacterium-mediated gene transfer by infiltration of adult Arabidopsis thaliana plants. Methods Mol Biol 82(10):259

    Google Scholar 

  • Bi G, Zhou Z, Wang W, Li L, Rao S, Wu Y, Zhang X, Menke FLH, Chen S, Zhou JM (2018) Receptor-like cytoplasmic kinases directly link diverse pattern recognition receptors to the activation of mitogen-activated protein kinase cascades in Arabidopsis. Plant Cell 30:1543–1561

    PubMed  PubMed Central  CAS  Google Scholar 

  • Catala R, Ouyang J, Abreu IA, Xu Y, Seo H, Zhang X, Chua NH (2007) The Arabidopsis E3 SUMO ligase SIZ1 regulates plant growth and drought responses. Plant Cell 19(9):2952–2966

    PubMed  PubMed Central  CAS  Google Scholar 

  • Choi SW, Lee SB, Na YJ, Jeung SG, Kim SY (2017) Arabidopsis MAP3K16 and other salt-inducible MAP3Ks regulate ABA response redundantly. Mol Cells 40(3):230–242

    PubMed  PubMed Central  CAS  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    PubMed  CAS  Google Scholar 

  • Danquah A, De ZA, Colcombet J, Hirt H (2014) The role of ABA and MAPK signaling pathways in plant abiotic stress responses. Biotechnol Adv 32(1):40–52

    PubMed  CAS  Google Scholar 

  • Danquah A, Zélicourt A, Boudsocq M, Neubauer J, Frei Dit Frey N, Leonhardt N, Pateyron S, Gwinner F, Tamby JP, Ortiz-Masia D, Marcote MJ, Hirt H, Colcombet J (2015) Identification and characterization of an ABA-activated MAP kinase cascade in Arabidopsis thaliana. Plant J 82(2):232–244

    PubMed  CAS  Google Scholar 

  • Fiil BK, Petersen K, Petersen M, Mundy J (2009) Gene regulation by MAP kinase cascades. Curr Opin Plant Bio 12(5):615–621

    CAS  Google Scholar 

  • Guan LM, Zhao J, Scandalios JG (2000) Cis-elements and trans-factors that regulate expression of the maize Cat1 antioxidant gene in response to ABA and osmotic stress: H2O2 is the likely intermediary signaling molecule for the response. Plant J 22(2):87–95

    PubMed  CAS  Google Scholar 

  • Gudesblat GE, Iusem ND, Morris PC (2007) Guard cell-specific inhibition of Arabidopsis MPK3 expression causes abnormal stomatal responses to abscisic acid and hydrogen peroxide. New Phytol 173(4):713–721

    PubMed  CAS  Google Scholar 

  • Halder V, Kombrink E (2015) Facile high-throughput forward chemical genetic screening by in situ monitoring of glucuronidase-based reporter gene expression in Arabidopsis thaliana. Front Plant Sci 6(13):1–12

    Google Scholar 

  • Jammes F, Song C, Shin D, Munemasa S, Takeda K, Gu D, Cho D, Lee S, Giordo R, Sritubtim S, Leonhardt N, Ellis BE, Murata Y, Kwak JM (2009) MAP kinases MPK9 and MPK12 are preferentially expressed in guard cells and positively regulate ROS-mediated ABA signaling. Proc Natl Acad Sci USA 106(48):20520–20525

    PubMed  CAS  Google Scholar 

  • Jia L, Sheng Z, Xu W, Li Y, Liu Y, Xia Y, Zhang J (2012) Modulation of anti-oxidation ability by proanthocyanidins during germination of Arabidopsis thaliana seeds. Mol Plant 5:472–481

    PubMed  CAS  Google Scholar 

  • Jiang M, Zhang J (2001) Effect of abscisic acid on active oxygen species, antioxidative defence system and oxidative damage in leaves of maize seedlings. Plant Cell Physiol 42(11):1265–1273

    PubMed  CAS  Google Scholar 

  • Kim D, Cho YH, Ryu H, Kim Y, Kim TH, Hwang I (2013) BLH1 and KNAT3 modulate ABA responses during germination and early seedling development in Arabidopsis. Plant J 75(5):755–766

    PubMed  CAS  Google Scholar 

  • Kovtun Y, Chiu WL, Tena G, Sheen J (2000) Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc Natl Acad Sci USA 97:2940–2945

    PubMed  CAS  Google Scholar 

  • Lampard GR, Lukowitz W, Ellis BE, Bergmann DC (2009) Novel and expanded roles for MAPK signaling in Arabidopsis stomatal cell fate revealed by cell type-specific manipulations. Plant Cell 21:3506–3517

    PubMed  PubMed Central  CAS  Google Scholar 

  • Li W, De CO, Dodd IC (2018) Long-distance ABA transport can mediate distal tissue responses by affecting local ABA concentrations. J Integr Plant Biol 60(1):16–33

    PubMed  CAS  Google Scholar 

  • Liu Y (2012) Roles of mitogen-activated protein kinase cascades in ABA signaling. Plant Cell Rep 31:1–12

    PubMed  Google Scholar 

  • Liu Y, Ye N, Liu R, Chen M, Zhang J (2010) H2O2 mediates the regulation of ABA catabolism and GA biosynthesis in Arabidopsis seed dormancy and germination. J Exp Bot 61(11):2979–2990

    PubMed  PubMed Central  CAS  Google Scholar 

  • MAPK Group (2002) Mitogen-activated protein kinase cascades in plants: a new nomenclature. Trends Plant Sci 7(7):301–308

    Google Scholar 

  • Matsuoka D, Yasufuku T, Furuya T, Nanmori T (2015) An abscisic acid inducible Arabidopsis MAPKKK, MAPKKK18 regulates leaf senescence via its kinase activity. Plant Mol Biol 87(6):565–575

    PubMed  CAS  Google Scholar 

  • Meng L, Yao S (2015) Transcription co-activator Arabidopsis ANGUSTIFOLIA3 (AN3) regulates water-use efficiency and drought tolerance by modulating stomatal density and improving root architecture by the transrepression of YODA (YDA). Plant Biotechnol J 13(7):893–902

    PubMed  CAS  Google Scholar 

  • Mishra G, Zhang W, Deng F, Zhao J, Wang X (2006) A bifurcating pathway directs abscisic acid effects on stomatal closure and opening in Arabidopsis. Science 312(5771):264–266

    PubMed  CAS  Google Scholar 

  • Nakashima K, Yamaguchishinozaki K (2013) ABA signaling in stress-response and seed development. Plant Cell Rep 32(7):959–970

    PubMed  CAS  Google Scholar 

  • Quarrie SA, Whitford PN, Appleford NEJ, Wang TL, Cook SK, Henson IE, Loveys BR (1988) A monoclonal antibody to (s)-abscisic acid: its characterisation and use in a radioimmunoassay for measuring abscisic acid in crude extracts of cereal and lupin leaves. Planta 173(3):330–339

    PubMed  CAS  Google Scholar 

  • Shu K, Liu XD, Xie Q, He ZH (2016) Two faces of one seed: hormonal regulation of dormancy and germination. Mol Plant 9(1):34–45

    PubMed  CAS  Google Scholar 

  • Su SH, Krysan PJ (2016) A double-mutant collection targeting map kinase related genes in Arabidopsis for studying genetic interactions. Plant J 88(5):867–878

    PubMed  CAS  Google Scholar 

  • Tajdel M, Mituła F, Ludwików A (2016) Regulation of Arabidopsis MAPKKK18 by ABI1 and SnRK2, components of the ABA signaling pathway. Plant Signal Behav 11(4):e1139277

    PubMed  PubMed Central  Google Scholar 

  • Umezawa T, Sugiyama N, Takahashi F, Anderson JC, Ishihama Y, Peck SC, Shinozaki K (2013) Genetics and Phosphoproteomics Reveal a Protein Phosphorylation Network in the Abscisic Acid Signaling Pathway in Arabidopsis thaliana. Sci Signal 6(270):rs8

    PubMed  Google Scholar 

  • Wang H, Ngwenyama N, Liu Y, Walker JC, Zhang S (2007) Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. Plant Cell 19:63–73

    PubMed  PubMed Central  Google Scholar 

  • Wu Y, Li Y, Liu Y, Xie Q (2015) Cautionary notes on the usage of abi1-2 and abi1-3 mutants of Arabidopsis ABI1 for functional studies. Mol Plant 8(2):335–338

    PubMed  CAS  Google Scholar 

  • Xi D, Liu W, Yang G, Wu C, Zheng C (2010) Seed-specific overexpression of antioxidant genes in arabidopsis enhances oxidative stress tolerance during germination and early seedling growth. Plant Biotechnol J 8(7):796–806

    PubMed  CAS  Google Scholar 

  • Xing Y, Jia W, Zhang J (2007) AtMEK1 mediates stress-induced gene expression of CAT1 catalase by triggering H2O2 production in Arabidopsis. J Exp Bot 58(11):2969–2981

    PubMed  CAS  Google Scholar 

  • Xing Y, Jia W, Zhang J (2008) AtMKK1 mediates ABA-induced CAT1 expression and H2O2 production via AtMPK6-coupled signaling in Arabidopsis. Plant J 54(3):440–451

    PubMed  CAS  Google Scholar 

  • Ye N, Zhu G, Liu Y, Li Y, Zhang J (2011) ABA controls H2O2 accumulation through the induction of OsCATB in rice leaves under water stress. Plant Cell Physiol 52(4):689–698

    PubMed  CAS  Google Scholar 

  • Yoshida T, Mogami J, Yamaguchishinozaki K (2014) ABA-dependent and ABA-independent signaling in response to osmotic stress in plants. Curr Opin Plant Bio 21(21C):133–139

    CAS  Google Scholar 

  • Zelicourt AD, Colcombet J, Hirt H (2016) The role of MAPK modules and ABA during abiotic stress signaling. Trends Plant Sci 21(8):677–685

    PubMed  Google Scholar 

  • Zhang A, Jiang M, Zhang J, Tan M, Hu X (2006) Mitogen-activated protein kinase is involved in abscisic acid-induced antioxidant defense and acts downstream of reactive oxygen species production in leaves of maize plants. Plant Physiol 141:475–487

    PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang A, Jiang JH, Ding HD, Xu SC, Hu XL, Tan MP (2007) Nitric oxide induced by hydrogen peroxide mediates abscisic acid-induced activation of the mitogen-activated protein kinase cascade involved in antioxidant defense in maize leaves. N Phytol 175(1):36–50

    CAS  Google Scholar 

  • Zhang H, Liu Y, Feng W, Yao D, Wang L, Guo J, Ni L, Zhang A, Tan M, Jiang M (2014) A novel rice C2H2-type zinc finger protein, ZFP36, is a key player involved in abscisic acid-induced antioxidant defence and oxidative stress tolerance in rice. J Exp Bot 65(20):5795–5809

    PubMed  PubMed Central  CAS  Google Scholar 

  • Zhao C, Wang P, Si T, Hsu CC, Wang L, Zayed O, Yu Z, Zhu Y, Dong J, Tao WA, Zhu JK (2017) Map kinase cascades regulate the cold response by modulating ICE1 protein stability. Dev Cell 43(5):618–829

    PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful for grant support from the Excellent Young Scientist Foundation of Henan University (yqpy20140030) and the Doctoral Fund of Hohhot University for Nationalities (HMBS1706).

Author information

Author notes

  1. Liguo Jia and Yuzhen Chen contributed equally to this work.

Authors and Affiliations

  1. College of Agronomy, Inner Mongolia Agricultural University, Hohhot, 010019, China

    Liguo Jia & Mingshou Fan

  2. Department of Environmental Engineering, Hohhot University for Nationalities, Hohhot, 010051, China

    Yuzhen Chen

  3. School of Life Sciences, Henan University, Kaifeng, 475004, China

    Wenrao Li

  4. Department of Biology, Hong Kong Baptist University, Hong Kong, China

    Jianhua Zhang

Authors
  1. Liguo Jia
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yuzhen Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mingshou Fan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Wenrao Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jianhua Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Concept and experimental design: WL, LJ. Experimental work: LJ and YC with technical guidance from JZ, MF, and WL. Data analysis: LJ. Manuscript preparation: LG and YC with editorial contributions from WL. All authors have read and approved the submitted manuscript.

Corresponding author

Correspondence to Wenrao Li.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jia, L., Chen, Y., Fan, M. et al. MAP3Kθ1 is Involved in Abscisic Acid Signaling in Drought Tolerance and Seed Germination in Arabidopsis. J. Plant Biol. 63, 11–21 (2020). https://doi.org/10.1007/s12374-020-09226-w

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12374-020-09226-w

Keywords

Search

Navigation