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Overexpression of RSOsPR10, a root-specific rice PR10 gene, confers tolerance against drought stress in rice and drought and salt stresses in bentgrass

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Abstract

RSOsPR10 was originally identified as a rice root-specific pathogenesis-related protein whose production was induced by drought and salinity stresses, but not by low temperature or abscisic acid. Our previous studies revealed that RSOsPR10 expression is up-regulated by jasmonic acid, and strongly inhibited by salicylic acid. Immunohistochemical experiments indicated RSOsPR10 is expressed in the root cortical cells. In the present study, we generated RSOsPR10-overexpressing lines of rice and bentgrass to examine the physiological roles of RSOsPR10 in plants. RSOsPR10-overexpressing rice plants were highly tolerant against drought stress, but not against salinity. In contrast, RSOsPR10-overexpressing bentgrass plants were tolerant against drought and salinity stresses. There was little difference between transgenic and wild-type plants regarding phenotype or above-ground growth rates. However, the root mass of the transgenic rice and bentgrass plants was significantly greater than that of the wild-type plants. Therefore, RSOsPR10 is likely involved in mediating environmental stress tolerance through an increase in root growth and development.

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References

  • Abenavoli RM, Leone M, Sunseri F, Bacchi M, Sorgona A (2016) Root phenotyping for drought tolerance in bean landraces from Calabria (Italy). J Agron Crop Sci 202:1–12

    Article  Google Scholar 

  • Agarwal P, Agarwal PK (2014) Pathogenesis related-10 proteins are small, structurally similar but with diverse role in stress signaling. Mol Biol Rep 41:599–611

    Article  CAS  PubMed  Google Scholar 

  • Ahmed NU, Park JI, Jung HJ, Seo MS, Kumar TS, Lee IH, Nou IS (2012) Identification and characterization of stress resistance related genes of Brassica rapa. Biotechnol Lett 34:979–987

    Article  CAS  PubMed  Google Scholar 

  • Akama K, Shiraishi H, Ohta S, Nakamura K, Okada K, Shimura Y (1992) Efficient transformation of Arabidopsis thaliana: comparison of the efficiencies with various organs, plant ecotypes and Agrobacterium strains. Plant Cell Rep 12:7–11

    Article  CAS  PubMed  Google Scholar 

  • Cai R, Zhao Y, Wang Y, Lin Y, Peng X, Li Q, Chang Y, Jiang H, Xiang Y, Cheng B (2014) Overexpression of a maize WRKY58 gene enhances drought and salt tolerance in transgenic rice. Plant Cell, Tissue Organ Cult 119:565–577

    Article  CAS  Google Scholar 

  • Casañal A, Zander U, Muñoz C, Dupeux F, Luque I, Botella MA, Schwab W, Valpuesta V, Marquez JA (2013) The strawberry pathogenesis-related 10 (PR-10) Fra a proteins control flavonoid biosynthesis by binding to metabolic intermediates. J Biol Chem 288:35322–35332

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen L, Jiang B, Wu C, Sun S, Hou W, Han T (2015) The characterization of GmTIP, a root-specific gene from soybean, and the expression analysis of its promoter. Plant Cell, Tissue Organ Cult 121:259–274

    Article  CAS  Google Scholar 

  • Chwastyk M, Jaskolski M, Cieplak M (2014) Structure-based analysis of thermodynamic and mechanical properties of cavity-containing proteins - case study of plant pathogenesis-related proteins of class 10. FEBS J 281:416–429

    Article  CAS  PubMed  Google Scholar 

  • Fattorini L, Falasca G, Kevers C, Rocca LM, Zadra C, Altamura MM (2009) Adventitious rooting is enhanced by methyl jasmonate in tobacco thin cell layers. Planta 231:155–168

    Article  CAS  PubMed  Google Scholar 

  • Fernandes H, Pasternak O, Bujacz G, Bujacz A, Sikorski MM, Jaskolski M (2008) Lupinus luteus pathogenesis-related protein as a reservoir for cytokinin. J Mol Biol 378:1040–1051

    Article  CAS  PubMed  Google Scholar 

  • Fernandes H, Michalska K, Sikorski M, Jaskolski M (2013) Structural and functional aspects of PR-10 proteins. FEBS J 280:1169–1199

    Article  CAS  PubMed  Google Scholar 

  • Gutierrez L, Mongelard G, Floková K, Pǎcurar DI, Novák O, Staswick P, Kowalczyk M, Pǎcurar M, Demailly H, Geiss G, Bellini C (2012) Auxin controls Arabidopsis adventitious root initiation by regulating jasmonic acid homeostasis. Plant Cell 24:2515–2527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hashimoto M, Kisseleva L, Sawa S, Furukawa T, Komatsu S, Koshiba T (2004) A novel rice PR10 protein, RSOsPR10, specifically induced in roots by biotic and abiotic stresses, possibly via the jasmonic acid signaling pathway. Plant Cell Physiol 45:550–559

    Article  CAS  PubMed  Google Scholar 

  • Hentrich M, Böttcher C, Düchting P, Cheng Y, Zhao Y, Berkowitz O, Masle J, Medina J, Pollmann S (2013) The jasmonic acid signaling pathway is linked to auxin homeostasis through the modulation of YUCCA8 and YUCCA9 gene expression. Plant J 74:626–637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hood EE, Helmer GL, Fraley RT, Chilton MD (1986) The hypervirulence of Agrobacterium tumefaciens A281 is encoded in a region of pTiBo542 outside of T-DNA. J Bacteriol 168:1291–1301

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jain S, Srivastava S, Sarin NB, Kav NN (2006) Proteomics reveals elevated levels of PR 10 proteins in saline-tolerant peanut (Arachis hypogaea) calli. Plant Physiol Biochem 44:253–259

    Article  CAS  PubMed  Google Scholar 

  • Jain S, Kumar D, Jain M, Chaudhary P, Deswal R, Sarin NB (2012) Ectopic overexpression of a salt stress-induced pathogenesis-related class 10 protein (PR10) gene from peanut (Arachis hypogaea L.) affords broad spectrum abiotic stress tolerance in transgenic tobacco. Plant Cell, Tissue Organ Cult 109:19–31

    Article  CAS  Google Scholar 

  • Jan A, Yang G, Nakamura H, Ichikawa H, Kitano H, Matsuoka M, Matsumoto H, Komatsu S (2004) Characterization of a xyloglucan endotransglucosylase gene that is up-regulated by gibberellin in rice. Plant Physiol 136:3670–3681

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim ST, Yu S, Kang YH, Kim SG, Kim JY, Kim SH, Kang KY (2008) The rice pathogen-related protein 10 (JIOsPR10) is induced by abiotic and biotic stresses and exhibits ribonuclease activity. Plant Cell Rep 27:593–603

    Article  CAS  PubMed  Google Scholar 

  • Lebel S, Schellenbaum P, Walter B, Maillot P (2010) Characterisation of the Vitis vinifera PR10 multigene family. BMC Plant Biol 10:184

    Article  PubMed  PubMed Central  Google Scholar 

  • Lee EJ, Facchini P (2010) Norcoclaurine synthase is a member of the pathogenesis-related 10/Bet v1 protein family. Plant Cell 22:3489–3503

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee OR, Kim YJ, Balusamy SR, Khorolragchaa A, Sathiyaraj G, Kim MK, Yang DC (2012a) Expression of the ginseng PgPR10-1 in Arabidopsis confers resistance against fungal and bacterial infection. Gene 506:85–92

    Article  CAS  PubMed  Google Scholar 

  • Lee OR, Pulla RK, Kim YJ, Balusamy SR, Yang DC (2012b) Expression and stress tolerance of PR10 genes from Panax ginseng C. A. Meyer. Mol Biol Rep 39:2365–2374

    Article  CAS  PubMed  Google Scholar 

  • Liu JJ, Ekramoddoullah AKM (2006) The family 10 of plant pathogenesis-related proteins: their structure, regulation, and function in response to biotic and abiotic stresses. Physiol Mol Plant Pathol 68:3–13

    Article  CAS  Google Scholar 

  • Liu X, Huang B, Lin J, Fei J, Chen Z, Pang Y, Sun X, Tang K (2006) A novel pathogenesis-related protein (SsPR10) from Solanum surattense with ribonucleolytic and antimicrobial activity is stress- and pathogen-inducible. J Plant Physiol 163:546–556

    Article  CAS  PubMed  Google Scholar 

  • Lu J, Robert CAM, Riemann M, Cosme M, Mène-Saffrané L, Massana J, Stout MJ, Lou Y, Gershenzon J, Erb M (2015) Induced jasmonate signaling leads to contrasting effects on root damage and herbivore performance. Plant Physiol 167:1100–1116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324:1064–1068

    CAS  PubMed  Google Scholar 

  • Mogensen JE, Ferreras M, Wimmer R, Petersen SV, Enghild JJ, Otzen DE (2007) The major allergen from birch tree pollen, Bet v 1, binds and permeabilizes membranes. Biochemistry 46:3356–3365

    Article  CAS  PubMed  Google Scholar 

  • Mohammadi M, Srivastava S, Hall JC, Kav NNV, Deyholos MK (2012) Two wheat (Triticum aestivum) pathogenesis-related 10 (PR-10) transcripts with distinct patterns of abundance in different organs. Mol Biotechnol 51:103–108

    Article  CAS  PubMed  Google Scholar 

  • Moons A, Prinsen E, Bauw G, Van Montagu M (1997) Antagonistic effects of abscisic acid and jasmonates on salt stress-inducible transcripts in rice roots. Plant Cell 12:2243–2259

    Article  Google Scholar 

  • Park CJ, Kim KJ, Shin R, Park JM, Shin YC, Paek KH (2004) Pathogenesis-related protein 10 isolated from hot pepper functions as a ribonuclease in an antiviral pathway. Plant J 37:186–198

    Article  CAS  PubMed  Google Scholar 

  • Pasternak O, Bujacz GD, Fujimoto Y, Hashimoto Y, Jelen F, Otlewski J, Sikorski MM, Jaskolski M (2006) Crystal structure of Vigna radiata cytokinin-specific binding protein in complex with zeatin. Plant Cell 18:2622–2634

    Article  PubMed  PubMed Central  Google Scholar 

  • Pnueli L, Hallak-Herr E, Rozenberg M, Cohen M, Goloubinoff P, Kaplan A, Mittler R (2002) Molecular and biochemical mechanisms associated with dormancy and drought tolerance in the desert legume Retama raetam. Plant J 31:319–330

    Article  CAS  PubMed  Google Scholar 

  • Pulla RK, Lee OR, In JG, Kim YJ, Senthil K, Yang DC (2010) Expression and functional characterization of pathogenesis-related protein family 10 gene, PgPR10-2, from Panax ginseng C.A. Meyer. Physiol Mol Plant Pathol 74:323–329

    Article  CAS  Google Scholar 

  • Radauer C, Lackner P, Breiteneder H (2008) The Bet v 1 fold: an ancient, versatile scaffold for binding of large, hydrophobic ligands. BMC Evol Biol 8:286

    Article  PubMed  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

    Article  PubMed  Google Scholar 

  • Rustagi A, Jain S, Kumar D, Shekhar S, Jain M, Bhat V, Sarin NB (2015) High efficiency transformation of banana [Musa acuminata L. cv. Matti (AA)] for enhanced tolerance to salt and drought stress through overexpression of a peanut salinity-induced pathogenesis-related class 10 protein. Mol Biotechnol 57:27–35

    Article  CAS  PubMed  Google Scholar 

  • Sallaud C, Gay C, Larmande P, Bès M, Piffanelli P, Piégu B, Droc G, Regad F, Bourgeois E, Meynard D, Périn C, Sabau X, Ghesquière A, Glaszmann JC, Delseny M, Guiderdoni E (2004) High throughput T-DNA insertion mutagenesis in rice: a first step towards in silico reverse genetics. Plant J 39:450–464

    Article  CAS  PubMed  Google Scholar 

  • Srivastava S, Fristensky B, Kav NNV (2004) Constitutive expression of a PR10 protein enhances the germination of Brassica napus under saline conditions. Plant Cell Physiol 45:1320–1324

    Article  CAS  PubMed  Google Scholar 

  • Sun J, Xu Y, Ye S, Jiang H, Chen Q, Liu F, Zhou W, Chen R, Li X, Tietz O, Wu X, Cohen JD, Palme K, Li C (2009) Arabidopsis ASA1 is important for jasmonate-mediated regulation of auxin biosynthesis and transport during lateral root formation. Plant Cell 21:1495–1511

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takeuchi K, Gyohda A, Tominaga M, Kawakatsu M, Hatakeyama A, Ishii N, Shimaya K, Nishimura T, Riemann M, Nick P, Hashimoto M, Komano T, Endo A, Okamoto T, Jikumaru Y, Kamiya Y, Terakawa T, Koshiba T (2011) RSOsPR10 expression in response to environmental stresses is regulated antagonistically by jasmonate/ethylene and salicylic acid signaling pathways in rice roots. Plant Cell Physiol 52:1686–1696

    Article  CAS  PubMed  Google Scholar 

  • Terakawa T, Hasegawa H, Yamaguchi M (2005) Efficient Whisker-mediated gene transformation in a combination with supersonic treatment. Breed Sci 55:465–468

    Article  CAS  Google Scholar 

  • van Loon LC, Rep M, Pieterse CM (2006) Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol 44:135–162

    Article  PubMed  Google Scholar 

  • Walter MH, Liu J-W, Wünn J, Hess D (1996) Bean ribonuclease-like pathogenesis-related protein genes (Ypr10) display complex patterns of developmental, dark-induced and exogenous-stimulus-dependent expression. Eur J Biochem 239:281–293

    Article  CAS  PubMed  Google Scholar 

  • Xie YR, Chen ZY, Brown RL, Bhatnagar D (2010) Expression and functional characterization of two pathogenesis-related protein 10 genes from Zea mays. J Plant Physiol 167:121–130

    Article  CAS  PubMed  Google Scholar 

  • Zhao L, Ma LG, Wang ZS, Chen ML, Shen Y, Huang LQ (2015) Molecular cloning and characterization of a pathogenesis-related protein SmPR10-1 from Salvia miltiorrhiza. Acta Physiol Plant 37:205

    Article  Google Scholar 

  • Zubini P, Zambelli B, Musiani F, Ciurli S, Bertolini P, Baraldi E (2009) The RNA hydrolysis and the cytokinin binding activities of PR-10 proteins are differently performed by two isoforms of the Pru p 1 peach major allergen and are possibly functionally related. Plant Physiol 150:1235–1247

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We thank Dr. Kenzo Nakamura (Chubu Univ.) for providing the binary vector pIG121-Hm. This work was supported in part by a Grant from the Ministry of Agriculture, Forestry, and Fisheries of Japan (GMA0008).

Author contributions

TT, AG, and TK designed the study and wrote the manuscript. KT, HH, and SK completed the experiments. TO and KO provided technical support and advice.

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Authors and Affiliations

  1. Department of Biological Sciences, Tokyo Metropolitan University, 1-1 Minami-Osawa, Hachioji, Tokyo, 192-0397, Japan

    Kaoru Takeuchi, Atsuko Gyohda, Takashi Okamoto & Tomokazu Koshiba

  2. Central Research Laboratories, Hokko Chemical Industry Co. Ltd., Toda, Atsugi, Kanagawa, 243-0023, Japan

    Hisakazu Hasegawa & Teruhiko Terakawa

  3. National Institute of Crop Science, Kannondai, Tsukuba, Ibaraki, 305-8518, Japan

    Setsuko Komatsu

  4. Biotechnology Research Center, The University of Tokyo, Bunkyo-ku, Tokyo, 113-8657, Japan

    Kazunori Okada

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  1. Kaoru Takeuchi
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  2. Hisakazu Hasegawa
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  3. Atsuko Gyohda
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  4. Setsuko Komatsu
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Correspondence to Tomokazu Koshiba.

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Takeuchi, K., Hasegawa, H., Gyohda, A. et al. Overexpression of RSOsPR10, a root-specific rice PR10 gene, confers tolerance against drought stress in rice and drought and salt stresses in bentgrass. Plant Cell Tiss Organ Cult 127, 35–46 (2016). https://doi.org/10.1007/s11240-016-1027-0

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