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OsJAZ9 overexpression modulates jasmonic acid biosynthesis and potassium deficiency responses in rice

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Abstract

Key message

Enhanced bioactive JA (JA-Ile) accumulation in OsJAZ9 overexpressing rice helps plants tolerate K deficiency.

Abstract

Potassium (K) represents up to 10% of the plant’s total dry biomass, and its deficiency makes plants highly susceptible to both abiotic and biotic stresses. K shortage results in the inhibition of root and shoots growth, but the underlying mechanism of this response is unclear. Our RNA-Seq and qPCR analysis suggested leading roles for JA pathway genes under K deficiency in rice. Notably, K deficiency and JA application produced similar phenotypic and transcriptional responses. Here, we integrated molecular, physiological and morphological studies to analyze the role of OsJAZ9 in JA homeostasis and K deficiency responses. We raised OsJAZ9 over-expression, knockdown, transcriptional reporter, translational reporter and C-terminal deleted translational reporter lines in rice to establish the role of JA signaling in K ion homeostasis. JA profiling revealed significantly increased JA-Ile levels in OsJAZ9 OE lines under K deficiency. Furthermore, we established that OsJAZ9 overexpression and knockdown result in K deficiency tolerance and sensitivity, respectively, by modulating various K transporters and root system architecture. Our data provide evidence on the crucial roles of OsJAZ9 for improving K deficiency tolerance in rice by altering JA levels and JA responses.

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References

  • Ahmad I, Mian A, Maathuis FJM (2016) Overexpression of the rice AKT1 potassium channel affects potassium nutrition and rice drought tolerance. J Exp Bot 67:2689–2698

    CAS  PubMed Central  Google Scholar 

  • Armengaud P, Breitling R, Amtmann A (2004) The potassium-dependent transcriptome of Arabidopsis reveals a prominent role of jasmonic acid in nutrient signaling. Plant Physiol 136:2556–2576

    CAS  PubMed Central  Google Scholar 

  • Bandyopadhyay T, Mehra P, Hairat S, Giri J (2017) Morpho-physiological and transcriptome profiling reveal novel zinc deficiency-responsive genes in rice. Funct Integr Genomics 17:565–581

    CAS  Google Scholar 

  • Cai Q, Yuan Z, Chen M, Yin C, Luo Z, Zhao X, Liang W, Hu J, Zhang D (2014) Jasmonic acid regulates spikelet development in rice. Nat Commun 5:3476

    Google Scholar 

  • Chini A, Fonseca S, Fernández G et al (2007) The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448:666–671

    CAS  Google Scholar 

  • Egilla JN, Davies FT, Drew MC (2001) Effect of potassium on drought resistance of Hibiscus rosa-sinensis cv. Leprechaun: plant growth, leaf macro- and micronutrient content and root longevity. Plant Soil 229:213–224

    CAS  Google Scholar 

  • Elumalai RP, Nagpal P, Reed JW (2002) A mutation in the Arabidopsis KT2/KUP2 potassium transporter gene affects shoot cell expansion. Plant Cell 14:119–131

    CAS  PubMed Central  Google Scholar 

  • Feys BJF, Benedetti CE, Penfold CN, Turner JG (1994) Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen. Plant Cell 6:751–759

    CAS  PubMed Central  Google Scholar 

  • Fu J, Wu H, Ma S, Xiang D, Liu R, Xiong L (2017) OsJAZ1 Attenuates drought resistance by regulating JA and ABA signaling in rice. Front Plant Sci 8:2108

    PubMed Central  Google Scholar 

  • Gruber BD, Giehl RFH, Friedel S, von Wirén N (2013) Plasticity of the Arabidopsis root system under nutrient deficiencies. Plant Physiol 163:161–179

    CAS  PubMed Central  Google Scholar 

  • Hakata M, Muramatsu M, Nakamura H et al (2017) Overexpression of TIFY genes promotes plant growth in rice through jasmonate signaling. Biosci Biotechnol Biochem 81:906–913

    CAS  Google Scholar 

  • Hardter R (2002) Potassium and biotic stress of plants. In: Johnston AE (ed) Feed the soil to feed the people. The role of potash in sustainable agriculture. International Potash Institute, Basel, pp 345–362

    Google Scholar 

  • Heitz T, Smirnova E, Widemann E, Aubert Y, Pinot F, Ménard R (2016) The rise and fall of jasmonate biological activities. Subcell Biochem 86:405–426

    CAS  Google Scholar 

  • Hickman R, Van Verk MC, Van Dijken AJH et al (2017) Architecture and dynamics of the jasmonic acid gene regulatory network. Plant Cell 29:2086–2105

    CAS  PubMed Central  Google Scholar 

  • Hsu YY, Kao CH (2011) Nitric oxide is involved in methyl jasmonate-induced lateral root formation in rice. Crop Environ Bioinform 8:160–167

    Google Scholar 

  • Kader MA, Seidel T, Golldack D, Lindberg S (2006) Expressions of OsHKT1, OsHKT2, and OsVHA are differentially regulated under NaCl stress in salt-sensitive and salt-tolerant rice (Oryza sativa L.) cultivars. J Exp Bot 57:4257–4268

    CAS  Google Scholar 

  • Kant S, Kafkafi U (2002) Potassium and abiotic stresses in plants. In: Pasricha NS, Bansal SK (eds) Potassium for sustainable crop production. Potash Institute of India, Gurgaon, pp 233–251

    Google Scholar 

  • Kaya C, Kirnak H, Higgs D (2006) Enhancement of growth and normal growth parameters by foliar application of potassium and phosphorus in tomato cultivars grown at high (NaCl) salinity. J Plant Nutr 24:357–367

    Google Scholar 

  • Kazan K (2015) Diverse roles of jasmonates and ethylene in abiotic stress tolerance. Trends Plant Sci 20:219–229

    CAS  Google Scholar 

  • Kobayashi T, Itai RN, Senoura T, Oikawa T, Ishimaru Y, Ueda M, Nakanishi H, Nishizawa NK (2016) Jasmonate signaling is activated in the very early stages of iron deficiency responses in rice roots. Plant Mol Biol 91:533–547

    CAS  PubMed Central  Google Scholar 

  • Leigh RA, Wyn Jones RG (1984) A hypothesis relating critical potassium concentrations for growth to the distribution and functions of this ion in the plant cell. New Phytol 97:1–13

    CAS  Google Scholar 

  • Li G, Wu Y, Liu G et al (2017) Large-scale proteomics combined with transgenic experiments demonstrates an important role of jasmonic acid in potassium deficiency response in wheat and rice. Mol Cell Proteomics 16:1889–1905

    CAS  PubMed Central  Google Scholar 

  • Ma TL, Wu WH, Wang Y (2012) Transcriptome analysis of rice root responses to potassium deficiency. BMC Plant Biol 12:161

    CAS  PubMed Central  Google Scholar 

  • Mann DG, LaFayette PR, Abercrombie LL et al (2012) Gateway-compatible vectors for high-throughput gene functional analysis in switchgrass (Panicum virgatum L.) and other monocot species. Plant Biotechnol J 10:226–236

    CAS  Google Scholar 

  • Mehra P, Giri J (2016) Rice and chickpea GDPDs are preferentially influenced by low phosphate and CaGDPD1 encodes an active glycerophosphodiester phosphodiesterase enzyme. Plant Cell Rep 35:1699–1717

    CAS  Google Scholar 

  • Mehra P, Pandey BK, Giri J (2017) Improvement in phosphate acquisition and utilization by a secretory purple acid phosphatase (OsPAP21b) in rice. Plant Biotechnol J 15:1054–1067

    CAS  PubMed Central  Google Scholar 

  • Mengel K, Viro M (1974) Effect of potassium supply on the transport of photosynthates to the fruits of tomatoes (Lycopersicon esculentum). Physiol Plant 30:295–300

    CAS  Google Scholar 

  • Nguyen HT, To HTM, Lebrun M, Bellafiore S, Champion A (2019) Jasmonates—the master regulator of rice development, adaptation and defense. Plants 8:339

    CAS  Google Scholar 

  • Oh Y, Baldwin IT, GÃlis I (2012) NaJAZh regulates a subset of defense responses against herbivores and spontaneous leaf necrosis in Nicotiana attenuata plants. Plant Physiol 159:769–788

    CAS  PubMed Central  Google Scholar 

  • Pandey BK, Mehra P, Verma L, Bhadouria J, Giri J (2017) OsHAD1, a haloacid dehalogenase-like APase enhances phosphate accumulation. Plant Physiol 174:2316–2332

    CAS  PubMed Central  Google Scholar 

  • Qi Z, Spalding EP (2004) Protection of plasma membrane K+ transport by the salt overly sensitive1 Na+/H+ antiporter during salinity stress. Plant Physiol 136:2548–2555

    CAS  PubMed Central  Google Scholar 

  • Raya-González J, Pelagio-Flores R, López-Bucio J (2012) The jasmonate receptor COI1 plays a role in jasmonate-induced lateral root formation and lateral root positioning in Arabidopsis thaliana. J Plant Physiol 169:1348–1358

    PubMed Central  Google Scholar 

  • Rich CI (1964) Effect of cation size and ph on potassium exchange in nason soil. Soil Sci 98:100–106

    CAS  Google Scholar 

  • Rich CI, Black WR (1964) Potassium exchange as affected by cation size, pH and mineral structure. Soil Sci 97:384–390

    CAS  Google Scholar 

  • Riemann M, Dhakarey R, Hazman M, Miro B, Kohli A, Nick P (2015) Exploring jasmonates in the hormonal network of drought and salinity responses. Front Plant Sci 6:1077

    PubMed Central  Google Scholar 

  • Sarwar M (2012) Effects of potassium fertilization on population build up of rice stem borers (lepidopteron pests) and rice (Oryza sativa L.) yield. J Cereals Oilseeds 3:6–9

    CAS  Google Scholar 

  • Sawhney BL, Zelitch I (1969) Direct determination of potassium ion accumulation in guard cells in relation to stomatal opening in light. Plant Physiol 44:1350–1354

    CAS  PubMed Central  Google Scholar 

  • Shankar A, Singh A, Kanwar P, Srivastava AK, Pandey A, Suprasanna P, Kapoor S, Pandey GK (2013) Gene expression analysis of rice seedling under potassium deprivation reveals major changes in metabolism and signaling components. PLoS ONE 8:e70321

    CAS  PubMed Central  Google Scholar 

  • Sheard LB, Tan X, Mao H et al (2010) Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor. Nature 468:400–405

    CAS  PubMed Central  Google Scholar 

  • Singh AP, Pandey BK, Deveshwar P, Narnoliya L, Parida SK, Giri J (2015) JAZ repressors: potential involvement in nutrients deficiency response in rice and chickpea. Front Plant Sci 6:975

    PubMed Central  Google Scholar 

  • Sparks DL (1987) Potassium dynamics in soils. In: Stewart BA (ed) Advances in soil science. Springer, New York, pp 1–63

    Google Scholar 

  • Staswick PE, Su W, Howell SH (1992) Methyl jasmonate inhibition of root growth and induction of a leaf protein are decreased in an Arabidopsis thaliana mutant. Proc Natl Acad Sci USA 89:6837–6840

    CAS  Google Scholar 

  • Takehisa H, Sato Y, Antonio BA, Nagamura Y (2013) Global transcriptome profile of rice root in response to essential macronutrient deficiency. Plant Signal Behav 8:e24409

    PubMed Central  Google Scholar 

  • Terry N, Ulrich A (1973) Effects of potassium deficiency on the photosynthesis and respiration of leaves of sugar beet. Plant Physiol 51:783–786

    CAS  PubMed Central  Google Scholar 

  • Tester M, Blatt MR (1989) Direct measurement of K+ channels in thylakoid membranes by incorporation of vesicles into planar lipid bilayers. Plant Physiol 91:249–252

    CAS  PubMed Central  Google Scholar 

  • Thatcher LF, Cevik V, Grant M, Zhai B, Jones JD, Manners JM, Kazan K (2016) Characterization of a JAZ7 activation-tagged Arabidopsis mutant with increased susceptibility to the fungal pathogen Fusarium oxysporum. J Exp Bot 67:2367–2386

    CAS  PubMed Central  Google Scholar 

  • Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He SY, Howe GA, Browse J (2007) JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling. Nature 448:661–665

    CAS  Google Scholar 

  • Troufflard S, Mullen W, Larson TR, Graham IA, Crozier A, Amtmann A, Armengaud P (2010) Potassium deficiency induces the biosynthesis of oxylipins and glucosinolates in Arabidopsis thaliana. BMC Plant Biol 10:172

    PubMed Central  Google Scholar 

  • Vadassery J, Reichelt M, Hause B, Gershenzon J, Boland W, Mithöfer A (2012) CML42-mediated calcium signaling coordinates responses to Spodoptera herbivory and abiotic stresses in Arabidopsis. Plant Physiology 159:1159–1175

    CAS  PubMed Central  Google Scholar 

  • Wang M, Zheng Q, Shen Q, Guo S (2013) The critical role of potassium in plant stress response. Int J Mol Sci 14:7370–7390

    CAS  PubMed Central  Google Scholar 

  • Wasternack C, Hause B (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in annals of botany. Ann Bot 111:1021–1058

    CAS  PubMed Central  Google Scholar 

  • Wasternack C, Song S (2017) Jasmonates: biosynthesis, metabolism, and signaling by proteins activating and repressing transcription. J Exp Bot 68:1303–1321

    CAS  Google Scholar 

  • Wu W, Peters J, Berkowitz GA (1991) Surface charge-mediated effects of Mg2+ on K+ flux across the chloroplast envelope are associated with regulation of stromal pH and photosynthesis. Plant Physiol 97:580–587

    CAS  PubMed Central  Google Scholar 

  • Wu H, Ye H, Yao R, Zhang T, Xiong L (2015) OsJAZ9 acts as a transcriptional regulator in jasmonate signaling and modulates salt stress tolerance in rice. Plant Sci 232:1–12

    CAS  Google Scholar 

  • Yamada S, Kano A, Tamaoki D, Miyamoto A, Shishido H, Miyoshi S, Taniguchi S, Akimitsu K, Gomi K (2012) Involvement of OsJAZ8 in jasmonate-induced resistance to bacterial blight in rice. Plant Cell Physiol 53:2060–2072

    CAS  Google Scholar 

  • Yang DL, Yao J, Mei CS et al (2012) Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade. Proc Natl Acad Sci USA 109:E1192–E1200

    CAS  Google Scholar 

  • Ye H, Du H, Tang N, Li X, Xiong L (2009) Identification and expression profiling analysis of TIFY family genes involved in stress and phytohormone responses in rice. Plant Mol Biol 71:291–305

    CAS  Google Scholar 

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Acknowledgements

A.P.S., P.M., and B.K.P. acknowledge the research fellowship by UGC, CSIR, and DBT, respectively. We thank Dr. Vijayata Singh, CSSRI, Karnal, for help in K and Na estimation. J.G. acknowledges a grant from the INSA-young scientist project. We acknowledge the NIPGR metabolomics facility.

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Author notes

  1. Ajit Pal Singh and Bipin K. Pandey have equal contribution.

Authors and Affiliations

  1. National Institute of Plant Genome Research, Aruna Asaf Ali Marg, New Delhi, 110067, India

    Ajit Pal Singh, Bipin K. Pandey, Poonam Mehra & Jitender Giri

  2. Plant and Crop Science Division, School of Biosciences, University of Nottingham, Nottingham, UK

    Bipin K. Pandey

  3. Institut de Biologie Moléculaire des Plantes (IBMP) du CNRS, Université de Strasbourg, Strasbourg, France

    Thierry Heitz

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  1. Ajit Pal Singh
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Contributions

APS, BKP, and PM conducted experiments and analyzed data. JG designed the project, supervised experiments. APS, BKP, PM, TH, and JG wrote the manuscript.

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Correspondence to Jitender Giri.

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Singh, A.P., Pandey, B.K., Mehra, P. et al. OsJAZ9 overexpression modulates jasmonic acid biosynthesis and potassium deficiency responses in rice. Plant Mol Biol 104, 397–410 (2020). https://doi.org/10.1007/s11103-020-01047-2

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