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Leucine-Rich Repeat Receptor-Like Kinase FON1 Regulates Drought Stress and Seed Germination by Activating the Expression of ABA-Responsive Genes in Rice

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Abstract

Receptor-like kinases (RLKs) play important roles in regulating plant development and responses to various environmental stresses. FLORAL ORGAN NUMBER1 (FON1), a leucine-rich repeat receptor-like kinase, was reported to participate in the control of vegetative and reproductive development, but little is known about its function in response to abiotic stress in rice. Here, we reported that FON1 was involved in the regulation of water stress and seed germination process by mediating the expression of abscise acid (ABA)-responsive genes. FON1 was expressed mainly in root and shoot and could be induced by NaCl, drought, and ABA treatment. Transgenic plants overexpressing FON1 exhibited enhanced drought stress and reduced accumulation of H2O2 and malondialdehyde compared to the control. In contrast, RNAi-mediated disruption of FON1 resulted in decreased drought stress associated with the excessive ROS accumulation. At the transcription level, several stress-related and ABA-responsive genes, including LEA3, OsbZIP46, APX3, APX5, and CATB, were upregulated in transgenic plants overexpressing FON1, but correspondingly downregulated in RNAi plants. Moreover, overexpression of FON1 led to delayed seed germination, inhibited early root growth, and increased susceptibility to ABA, likely by activating the expression of ABA-responsive homeodomain transcription factors. These results provide new insight into the function of FON1 in the regulation of drought stress and early growth processes by tuning ABA signaling in rice.

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Abbreviations

ABA:

Abscise acid

APX3:

Ascorbate peroxidase 3

APX5:

Ascorbate peroxidase 5

CATB:

Catalases B

FON1:

FLORAL ORGAN NUMBER1

GUS:

Beta-Glucuronidase

LEA proteins:

Late embryogenesis abundant proteins

MDA:

Malondialdehyde

OE:

Overexpression

Ri:

RNA interference

ROS:

Reactive oxygen species

RLKs:

Receptor-like kinases

References

  • Akamatsu A, Wong HL, Fujiwara M, Okuda J, Nishide K, Uno K, Imai K, Umemura K, Kawasaki T, Kawano Y, Shimamoto K (2013) An OsCEBiP/OsCERK1-OsRacGEF1-OsRac1 module is an essential early component of chitin-induced rice immunity. Cell Host Microbe 13:465–476

    Article  PubMed  CAS  Google Scholar 

  • Antoni R, Gonzalez-Guzman M, Rodriguez L, Peirats-Llobet M, Pizzio GA, Fernandez MA, De Winne N, De Jaeger G, Dietrich D, Bennett MJ, Rodriguez PL (2013) PYRABACTIN RESISTANCE1-LIKE8 plays an important role for the regulation of abscisic acid signaling in root. Plant Physiol 161:931–941

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Arc E, Sechet J, Corbineau F, Rajjou L, Marion-Poll A (2013) ABA crosstalk with ethylene and nitric oxide in seed dormancy and germination. Front Plant Sci 4:63

    PubMed  PubMed Central  Google Scholar 

  • Asano T, Hakata M, Nakamura H, Aoki N, Komatsu S, Ichikawa H, Hirochika H, Ohsugi R (2011) Functional characterisation of OsCPK21, a calcium-dependent protein kinase that confers salt tolerance in rice. Plant Mol Biol 75:179–191

    Article  PubMed  CAS  Google Scholar 

  • Asano T, Hayashi N, Kikuchi S, Ohsugi R (2012a) CDPK-mediated abiotic stress signaling. Plant Signal Behav 7:817–821

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Asano T, Hayashi N, Kobayashi M, Aoki N, Miyao A, Mitsuhara I, Ichikawa H, Komatsu S, Hirochika H, Kikuchi S, Ohsugi R (2012b) A rice calcium-dependent protein kinase OsCPK12 oppositely modulates salt-stress tolerance and blast disease resistance. Plant J 69:26–36

    Article  PubMed  CAS  Google Scholar 

  • Chae MJ, Lee JS, Nam MH, Cho K, Hong JY, Yi SA, Suh SC, Yoon IS (2007) A rice dehydration-inducible SNF1-related protein kinase 2 phosphorylates an abscisic acid responsive element-binding factor and associates with ABA signaling. Plant Mol Biol 63:151–169

    Article  PubMed  CAS  Google Scholar 

  • Chen CW, Yang YW, Lur HS, Tsai YG, Chang MC (2006) A novel function of abscisic acid in the regulation of rice (Oryza sativa L.) root growth and development. Plant Cell Physiol 47:1–13

    Article  PubMed  Google Scholar 

  • Chu H, Liang W, Li J, Hong F, Wu Y, Wang L, Wang J, Wu P, Liu C, Zhang Q, Xu J, Zhang D (2013) A CLE-WOX signalling module regulates root meristem maintenance and vascular tissue development in rice. J Exp Bot 64:5359–5369

    Article  PubMed  CAS  Google Scholar 

  • Deak KI, Malamy J (2005) Osmotic regulation of root system architecture. Plant J 43:17–28

    Article  PubMed  CAS  Google Scholar 

  • Duan L, Dietrich D, Ng CH, Chan PM, Bhalerao R, Bennett MJ, Dinneny JR (2013) Endodermal ABA signaling promotes lateral root quiescence during salt stress in Arabidopsis seedlings. Plant Cell 25:324–341

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Fujii H, Zhu JK (2012) Osmotic stress signaling via protein kinases. Cell Mol Life Sci 69:3165–3173

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Fujita Y, Nakashima K, Yoshida T, Katagiri T, Kidokoro S, Kanamori N, Umezawa T, Fujita M, Maruyama K, Ishiyama K, Kobayashi M, Nakasone S, Yamada K, Ito T, Shinozaki K, Yamaguchi-Shinozaki K (2009) Three SnRK2 protein kinases are the main positive regulators of abscisic acid signaling in response to water stress in Arabidopsis. Plant Cell Physiol 50:2123–2132

    Article  PubMed  CAS  Google Scholar 

  • Fujita Y, Yoshida T, Yamaguchi-Shinozaki K (2013) Pivotal role of the AREB/ABF-SnRK2 pathway in ABRE-mediated transcription in response to osmotic stress in plants. Physiol Plant 147:15–27

    Article  PubMed  CAS  Google Scholar 

  • Fukao T, Yeung E, Bailey-Serres J (2011) The submergence tolerance regulator SUB1A mediates crosstalk between submergence and drought tolerance in rice. Plant Cell 23:412–427

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Gaudin AC, Henry A, Sparks AH, Slamet-Loedin IH (2013) Taking transgenic rice drought screening to the field. J Exp Bot 64:109–117

    Article  PubMed  CAS  Google Scholar 

  • Hadiarto T, Tran LS (2011) Progress studies of drought-responsive genes in rice. Plant Cell Rep 30:297–310

    Article  PubMed  CAS  Google Scholar 

  • Hand SC, Menze MA, Toner M, Boswell L, Moore D (2011) LEA proteins during water stress: not just for plants anymore. Annu Rev Physiol 73:115–134

    Article  PubMed  CAS  Google Scholar 

  • Hodges DM, DeLong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604–611

    Article  CAS  Google Scholar 

  • Hong CY, Hsu YT, Tsai YC, Kao CH (2007) Expression of ASCORBATE PEROXIDASE 8 in roots of rice (Oryza sativa L.) seedlings in response to NaCl. J Exp Bot 58:3273–3283

    Article  PubMed  CAS  Google Scholar 

  • Hong JH, Seah SW, Xu J (2013) The root of ABA action in environmental stress response. Plant Cell Rep 32:971–983

    Article  PubMed  CAS  Google Scholar 

  • Kim H, Hwang H, Hong JW, Lee YN, Ahn IP, Yoon IS, Yoo SD, Lee S, Lee SC, Kim BG (2012) A rice orthologue of the ABA receptor, OsPYL/RCAR5, is a positive regulator of the ABA signal transduction pathway in seed germination and early seedling growth. J Exp Bot 63:1013–1024

    Article  PubMed  CAS  Google Scholar 

  • Kim D., Cho Y.H., Ryu H., Kim Y., Kim T.H. & Hwang I. (2013) BLH1 and KNAT3 modulate ABA responses during germination and early seedling development in Arabidopsis. Plant J 32(7):1007–1016

    Google Scholar 

  • Kohli A, Sreenivasulu N, Lakshmanan P, Kumar PP (2013) The phytohormone crosstalk paradigm takes center stage in understanding how plants respond to abiotic stresses. Plant Cell Rep 32:945–957

    Article  PubMed  CAS  Google Scholar 

  • Lata C, Prasad M (2011) Role of DREBs in regulation of abiotic stress responses in plants. J Exp Bot 62:4731–4748

    Article  PubMed  CAS  Google Scholar 

  • Lu CA, Lin CC, Lee KW, Chen JL, Huang LF, Ho SL, Liu HJ, Hsing YI, Yu SM (2007) The SnRK1A protein kinase plays a key role in sugar signaling during germination and seedling growth of rice. Plant Cell 19:2484–2499

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Moon S, Jung KH, Lee DE, Lee DY, Lee J, An K, Kang HG, An G (2006) The rice FON1 gene controls vegetative and reproductive development by regulating shoot apical meristem size. Mol Cell 21:147–152

    CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Ohmori Y, Tanaka W, Kojima M, Sakakibara H, Hirano HY (2014) WUSCHEL-RELATED HOMEOBOX4 is involved in meristem maintenance and is negatively regulated by the CLE gene FCP1 in rice. Plant Cell 25:229–241

    Article  Google Scholar 

  • Osakabe Y, Yamaguchi-Shinozaki K, Shinozaki K. & Tran LS (2014) ABA control of plant macroelement membrane transport systems in response to water deficit and high salinity. New Phytol 202(1):35–49

    Google Scholar 

  • Osakabe Y, Yamaguchi-Shinozaki K, Shinozaki K, Tran LS (2013) Sensing the environment: key roles of membrane-localized kinases in plant perception and response to abiotic stress. J Exp Bot 64:445–458

    Article  PubMed  CAS  Google Scholar 

  • Ouyang SQ, Liu YF, Liu P, Lei G, He SJ, Ma B, Zhang WK, Zhang JS, Chen SY (2010) Receptor-like kinase OsSIK1 improves drought and salt stress tolerance in rice (Oryza sativa) plants. Plant J 62:316–329

    Article  PubMed  CAS  Google Scholar 

  • Park JJ, Yi J, Yoon J, Cho LH, Ping J, Jeong HJ, Cho SK, Kim WT, An G (2011) OsPUB15, an E3 ubiquitin ligase, functions to reduce cellular oxidative stress during seedling establishment. Plant J 65:194–205

    Article  PubMed  CAS  Google Scholar 

  • Piao HL, Xuan YH, Park SH, Je BI, Park SJ, Kim CM, Huang J, Wang GK, Kim MJ, Kang SM, Lee IJ, Kwon TR, Kim YH, Yeo US, Yi G, Son D, Han CD (2010) OsCIPK31, a CBL-interacting protein kinase is involved in germination and seedling growth under abiotic stress conditions in rice plants. Mol Cells 30:19–27

    Article  PubMed  CAS  Google Scholar 

  • Potters G, Pasternak TP, Guisez Y, Palme KJ, Jansen MA (2007) Stress-induced morphogenic responses: growing out of trouble? Trends Plant Sci 12:98–105

    Article  PubMed  CAS  Google Scholar 

  • Pu CX, Ma Y, Wang J, Zhang YC, Jiao XW, Hu YH, Wang LL, Zhu ZG, Sun D, Sun Y (2012) Crinkly4 receptor-like kinase is required to maintain the interlocking of the palea and lemma, and fertility in rice, by promoting epidermal cell differentiation. Plant J 70:940–953

    Article  PubMed  CAS  Google Scholar 

  • Rampitsch C, Bykova NV (2012) The beginnings of crop phosphoproteomics: exploring early warning systems of stress. Front Plant Sci 3:144

    Article  PubMed  PubMed Central  Google Scholar 

  • Rosa SB, Caverzan A, Teixeira FK, Lazzarotto F, Silveira JA, Ferreira-Silva SL, Abreu-Neto J, Margis R, Margis-Pinheiro M (2010) Cytosolic APx knockdown indicates an ambiguous redox responses in rice. Phytochemistry 71:548–558

    Article  PubMed  CAS  Google Scholar 

  • Santos AP, Serra T, Figueiredo DD, Barros P, Lourenco T, Chander S, Oliveira MM, Saibo NJ (2011) Transcription regulation of abiotic stress responses in rice: a combined action of transcription factors and epigenetic mechanisms. OMICS 15:839–857

    Article  PubMed  CAS  Google Scholar 

  • Sharp RE, Poroyko V, Hejlek LG, Spollen WG, Springer GK, Bohnert HJ, Nguyen HT (2004) Root growth maintenance during water deficits: physiology to functional genomics. J Exp Bot 55:2343–2351

    Article  PubMed  CAS  Google Scholar 

  • Shi B, Ni L, Zhang A, Cao J, Zhang H, Qin T, Tan M, Zhang J, Jiang M (2012) OsDMI3 is a novel component of abscisic acid signaling in the induction of antioxidant defense in leaves of rice. Mol Plant 5:1359–1374

    Article  PubMed  CAS  Google Scholar 

  • Shi B, Ni L, Liu Y, Zhang A, Tan M, Jiang M (2014) OsDMI3-mediated activation of OsMPK1 regulates the activities of antioxidant enzymes in abscisic acid signalling in rice. Plant Cell Environ 37(2):341–352

    Article  PubMed  CAS  Google Scholar 

  • Sreenivasulu N, Harshavardhan VT, Govind G, Seiler C, Kohli A (2012) Contrapuntal role of ABA: does it mediate stress tolerance or plant growth retardation under long-term drought stress? Gene 506:265–273

    Article  PubMed  CAS  Google Scholar 

  • Sun X, Wang GL (2011) Genome-wide identification, characterization and phylogenetic analysis of the rice LRR-kinases. PLoS One 6:e16079

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Suzaki T, Sato M, Ashikari M, Miyoshi M, Nagato Y, Hirano HY (2004) The gene FLORAL ORGAN NUMBER1 regulates floral meristem size in rice and encodes a leucine-rich repeat receptor kinase orthologous to Arabidopsis CLAVATA1. Development 131:5649–5657

    Article  PubMed  CAS  Google Scholar 

  • Tang N, Zhang H, Li X, Xiao J, Xiong L (2012) Constitutive activation of transcription factor OsbZIP46 improves drought tolerance in rice. Plant Physiol 158:1755–1768

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Teixeira FK, Menezes-Benavente L, Galvao VC, Margis R, Margis-Pinheiro M (2006) Rice ascorbate peroxidase gene family encodes functionally diverse isoforms localized in different subcellular compartments. Planta 224:300–314

    Article  PubMed  CAS  Google Scholar 

  • Wang N, Huang HJ, Ren ST, Li JJ, Sun Y, Sun DY, Zhang SQ (2012) The rice wall-associated receptor-like kinase gene OsDEES1 plays a role in female gametophyte development. Plant Physiol 160:696–707

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Wang P, Xue L, Batelli G, Lee S, Hou YJ, Van Oosten MJ, Zhang H, Tao WA, Zhu JK (2013) Quantitative phosphoproteomics identifies SnRK2 protein kinase substrates and reveals the effectors of abscisic acid action. Proc Natl Acad Sci U S A 110:11205–11210

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Xiao B, Huang Y, Tang N, Xiong L (2007) Over-expression of a LEA gene in rice improves drought resistance under the field conditions. Theor Appl Genet 115:35–46

    Article  PubMed  CAS  Google Scholar 

  • Xiong L, Yang Y (2003) Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acid-inducible mitogen-activated protein kinase. Plant Cell 15:745–759

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Yamaguchi K, Yamada K, Ishikawa K, Yoshimura S, Hayashi N, Uchihashi K, Ishihama N, Kishi-Kaboshi M, Takahashi A, Tsuge S, Ochiai H, Tada Y, Shimamoto K, Yoshioka H, Kawasaki T (2013) A receptor-like cytoplasmic kinase targeted by a plant pathogen effector is directly phosphorylated by the chitin receptor and mediates rice immunity. Cell Host Microbe 13:347–357

    Article  PubMed  CAS  Google Scholar 

  • Ye N, Zhu G, Liu Y, Li Y, Zhang J (2011) ABA controls H(2)O(2) accumulation through the induction of OsCATB in rice leaves under water stress. Plant Cell Physiol 52:689–698

    Article  PubMed  CAS  Google Scholar 

  • Zan Y, Ji Y, Zhang Y, Yang S, Song Y, Wang J (2013) Genome-wide identification, characterization and expression analysis of populus leucine-rich repeat receptor-like protein kinase genes. BMC Genomics 14:318

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Zhang Z, Zhang Q, Wu J, Zheng X, Zheng S, Sun X, Qiu Q, Lu T (2013) Gene knockout study reveals that cytosolic ascorbate peroxidase 2(OsAPX2) plays a critical role in growth and reproduction in rice under drought, salt and cold stresses. PLoS One 8:e57472

    Article  PubMed  CAS  PubMed Central  Google Scholar 

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Acknowledgments

This work was supported by the Grant Special Foundation of Transgenic Plants in China (2013ZX001-003 and 2014ZX08009-15B).

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Authors and Affiliations

  1. Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing, 100081, China

    Lei Feng, Zhenrui Gao, Guiqing Xiao, Rongfeng Huang & Haiwen Zhang

  2. National Key Facility of Crop Gene Resources and Genetic Improvement, Beijing, 100081, China

    Rongfeng Huang & Haiwen Zhang

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  1. Lei Feng
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  2. Zhenrui Gao
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  3. Guiqing Xiao
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  4. Rongfeng Huang
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  5. Haiwen Zhang
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Correspondence to Rongfeng Huang or Haiwen Zhang.

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Table Supplement 1

The list of primers used in this study (DOCX 18 kb)

Figure Supplement 1

Identification of the transgenic plants at the DNA and RNA levels. Analysis of the transgenic rice plants at the DNA level using PCR with specific primers corresponding to the hygromycin gene for the OE lines (A) and the NPTII gene for the Ri lines (B). (C) Analysis of FON1 expression in the leaves of 2-week-old seedlings from the OE, Ri, and WT plants using qPCR with specific primers for FON1. The expression levels in the transgenic plants are relative to the expression in WT plant (set as 1). OsActin1 was used as the internal control. The error bars (SD) are based on three independent experiments (GIF 49 kb)

High Resolution image (TIFF 2215 kb)

Figure Supplement 2

Seed germination in the Ri and WT plants. All seeds from the Ri and WT plants were placed on wet filter paper, immersed in water, and incubated at 30 °C. Their germination statuses were photographed at 96 h (GIF 30 kb)

High Resolution image (TIFF 1341 kb)

Figure Supplement 3

The effects of ABA and fluridone on seed germination in three OE lines. (A) ABA inhibited seed germination in the FON1 OE lines. The seeds were pretreated with 100 μM fluridone at 4 °C for 48 h and incubated with 0, 5, or 10 μM ABA solutions for 4 days. (B) For the fluridone treatment, all seeds were placed on wet filter paper with 0, 5, or 20 μM fluridone solutions for 4 days. The germination rates of the OE lines were calculated at 36, 48, 60, and 72 h relative to the germination rate of WT plants under the same conditions (GIF 19 kb)

High Resolution image (TIFF 3496 kb)

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Feng, L., Gao, Z., Xiao, G. et al. Leucine-Rich Repeat Receptor-Like Kinase FON1 Regulates Drought Stress and Seed Germination by Activating the Expression of ABA-Responsive Genes in Rice. Plant Mol Biol Rep 32, 1158–1168 (2014). https://doi.org/10.1007/s11105-014-0718-0

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