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Cotton S-adenosylmethionine decarboxylase-mediated spermine biosynthesis is required for salicylic acid- and leucine-correlated signaling in the defense response to Verticillium dahliae

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Abstract

Main conclusion

Cotton S-adenosylmethionine decarboxylase-, rather than spermine synthase-, mediated spermine biosynthesis is required for salicylic acid- and leucine-correlated signaling in the defense response to Verticillium dahliae.

Spermine (Spm) signaling is correlated with plant resistance to the fungal pathogen Verticillium dahliae. We identified genes for key rate-limiting enzymes in the biosynthesis of Spm, namely S-adenosylmethionine decarboxylase (GhSAMDC) and Spm synthase (GhSPMS). These were found by screening suppression subtractive hybridization and cDNA libraries of cotton (Gossypium) species tolerant to Verticillium wilt. Both were induced early and strongly by inoculation with V. dahliae and application of plant hormones. Silencing of GhSPMS or GhSAMDC in cotton leaves led to a significant accumulation of upstream substrates and, ultimately, enhanced plant susceptibility to Verticillium infection. Exogenous supplementation of Spm to the silenced cotton plants improved resistance. When compared with the wild type (WT), constitutive expression of GhSAMDC in Arabidopsis thaliana was associated with greater Verticillium wilt resistance and higher accumulations of Spm, salicylic acid, and leucine during the infection period. By contrast, transgenic Arabidopsis plants that over-expressed GhSPMS were unexpectedly more susceptible than the WT to V. dahliae and they also had impaired levels of putrescine (Put) and salicylic acid (SA). The susceptibility exhibited in GhSPMS-overexpressing Arabidopsis plants was partially reversed by the exogenous supply of Put or SA. In addition, the responsiveness of those two transgenic Arabidopsis lines to V. dahliae was associated with an alteration in transcripts of genes involved in plant resistance to epidermal penetrations and amino acid signaling. Together, these results suggest that GhSAMDC-, rather than GhSPMS-, mediated spermine biosynthesis contributes to plant resistance against V. dahliae through SA- and leucine-correlated signaling.

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Abbreviations

ACO2:

Amino cyclopropane carboxylate oxidase 2

AZI1:

Azelaic acid induced 1

EF-1α:

Elongation factor 1-alpha

EIN3:

Ethylene insensitive 3

ERF1:

Ethylene response factor 1

ET:

Ethylene

JA:

Jasmonic acid

LYS1:

Lysozyme 1

NPR1:

Nonexpressor of pathogenesis-related (PR) genes 1

ORA59:

Octadecanoid-responsive Arabidopsis AP2/ERF domain protein 59

PA:

Polyamine

PDF1.2:

Plant defensin 1.2

PME3:

Pectin methylesterase 3

Put:

Putrescine

SA:

Salicylic acid

SAMDC:

S-adenosylmethionine decarboxylase

Spd:

Spermidine

Spm:

Spermine

SPMS:

Spermine synthase

UBQ:

Ubiquitin

UGT:

UDP-glucosyltransferase

VIGS:

Virus-induced gene silencing

VSP2:

Vegetative storage protein 2

References

  • Bouché N, Fromm H (2004) GABA in plants: just a metabolite? Trends Plant Sci 9:110–115

    Article  PubMed  Google Scholar 

  • Breitenbach HH, Wenig M, Wittek F et al (2014) Contrasting roles of the apoplastic aspartyl protease APOPLASTIC, ENHANCED DISEASE SUSCEPTIBILITY1-DEPENDENT1 and LEGUME LECTIN-LIKE PROTEIN1 in Arabidopsis systemic acquired resistance. Plant Physiol 165:791–809

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choi DS, Hwang IS, Hwang BK (2012) Requirement of the cytosolic interaction between PATHOGENESIS-RELATED PROTEIN10 and LEUCINE-RICH REPEAT PROTEIN1 for cell death and defense signaling in pepper. Plant Cell 24:1675–1690

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • de Jonge R, van Esse HP, Maruthachalam K et al (2012) Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing. Proc Natl Acad Sci USA 109:5110–5115

    Article  PubMed  PubMed Central  Google Scholar 

  • Dewdney J, Reuber TL, Wildermuth MC et al (2000) Three unique mutants of Arabidopsis identify eds loci required for limiting growth of a biotrophic fungal pathogen. Plant J 24:205–218

    Article  CAS  PubMed  Google Scholar 

  • El Hadrami A, Adam LR, Daayf F (2011) Biocontrol treatments confer protection against Verticillium dahliae infection of potato by inducing antimicrobial metabolites. Mol Plant Microbe In 24:328–335

    Article  Google Scholar 

  • El Oirdi M, El Rahman TA, Rigano L et al (2011) Botrytis cinerea manipulates the antagonistic effects between immune pathways to promote disease development in tomato. Plant Cell 23:2405–2421

    Article  PubMed  PubMed Central  Google Scholar 

  • Ellendorff U, Fradin EF, de Jonge R et al (2009) RNA silencing is required for Arabidopsis defence against Verticillium wilt disease. J Exp Bot 60:591–602

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fellenberg C, Ziegler J, Handrick V et al (2012) Polyamine homeostasis in wild type and phenolamide deficient Arabidopsis thaliana stamens. Front Plant Sci 3:180

    Article  PubMed  PubMed Central  Google Scholar 

  • Fonseca S, Chini A, Hamberg M et al (2009) (+)-7-Isojasmonoyl-l-isoleucine is the endogenous bioactive jasmonate. Nat Chem Biol 5:344–350

    Article  CAS  PubMed  Google Scholar 

  • Gao X, Wheeler T, Li Z et al (2011) Silencing GhNDR1 and GhMKK2 compromises cotton resistance to Verticillium wilt. Plant J 66:293–305

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118

    Article  CAS  PubMed  Google Scholar 

  • Ge CM, Cui X, Wang Y et al (2006) BUD2, encoding an S-adenosylmethionine decarboxylase, is required for Arabidopsis growth and development. Cell Res 16:446–456

    Article  CAS  PubMed  Google Scholar 

  • Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez ME, Marco F, Minguet EG et al (2011) Perturbation of spermine synthase gene expression and transcript profiling provide new insights on the role of the tetraamine spermine in Arabidopsis defense against Pseudomonas viridiflava. Plant Physiol 156:2266–2277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grant JJ, Loake GJ (2000) Role of reactive oxygen intermediates and cognate redox signaling in disease resistance. Plant Physiol 124:21–29

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo H, Dang X, Dong J (2014) Hydrogen peroxide and nitric oxide are involved in salicylic acid-induced salvianolic acid B production in Salvia miltiorrhiza cell cultures. Molecules 19:5913–5924

    Article  PubMed  Google Scholar 

  • Hatmi S, Gruau C, Trotel-Aziz P et al (2015) Drought stress tolerance in grapevine involves activation of polyamine oxidation contributing to improved immune response and low susceptibility to Botrytis cinerea. J Exp Bot 66:775–787

    Article  CAS  PubMed  Google Scholar 

  • Hazarika P, Rajam MV (2011) Biotic and abiotic stress tolerance in transgenic tomatoes by constitutive expression of S-adenosylmethionine decarboxylase gene. Physiol Mol Biol Plants 17:115–128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heinrikson RL, Meredith SC (1984) Amino acid analysis by reverse-phase high-performance liquid chromatography: precolumn derivatization with phenylisothiocyanate. Anal Biochem 136:65–74

    Article  CAS  PubMed  Google Scholar 

  • Hewezi T, Howe P, Maier TR et al (2008) Cellulose binding protein from the parasitic nematode Heterodera schachtii interacts with Arabidopsis pectin methylesterase: cooperative cell wall modification during parasitism. Plant Cell 20:3080–3093

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu M, Pei BL, Zhang LF et al (2014) Histone H2B monoubiquitination is involved in regulating the dynamics of microtubules during the defense response to Verticillium dahliae toxins in Arabidopsis. Plant Physiol 164:1857–1865

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jung HW, Tschaplinski TJ, Wang L et al (2009) Priming in systemic plant immunity. Science 324:89–91

    Article  PubMed  Google Scholar 

  • Kim NH, Kim BS, Hwang BK (2013) Pepper arginine decarboxylase is required for polyamine and γ-aminobutyric acid signaling in cell death and defense response. Plant Physiol 162:2067–2083

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim DW, Watanabe K, Murayama C et al (2014) Polyamine oxidase5 regulates Arabidopsis growth through thermospermine oxidase activity. Plant Physiol 165:1575–1590

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klosterman SJ, Atallah ZK, Vallad GE et al (2009) Diversity, pathogenicity, and management of Verticillium species. Annu Rev Phytopathol 47:39–62

    Article  CAS  PubMed  Google Scholar 

  • Koomoa DL, Borsics T, Feith DJ et al (2009) Inhibition of S-adenosylmethionine decarboxylase by inhibitor SAM486A connects polyamine metabolism with p53-Mdm2-Akt/protein kinase B regulation and apoptosis in neuroblastoma. Mol Cancer Ther 8:2067–2075

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kurt S, Dervis S, Sahinler S (2003) Sensitivity of Verticillium dahliae to prochloraz and prochloraz-manganese complex and control of Verticillium wilt of cotton in the field. Crop Prot 22:51–55

    Article  CAS  Google Scholar 

  • Langenbach C, Campe R, Schaffrath U et al (2013) UDP-glucosyltransferase UGT84A2/BRT1 is required for Arabidopsis nonhost resistance to the Asian soybean rust pathogen Phakopsora pachyrhizi. New Phytol 198:536–545

    Article  CAS  PubMed  Google Scholar 

  • Leon J, Lawton MA, Raskin I (1995) Hydrogen peroxide stimulates salicylic acid biosynthesis in tobacco. Plant Physiol 108:1673–1678

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lievens B, Brouwer M, Vanachter ACRC et al (2006) Real-time PCR for detection and quantification of fungal and oomycete tomato pathogens in plant and soil samples. Plant Sci 171:155–165

    Article  CAS  Google Scholar 

  • Lionetti V (2015) PECTOPLATE: the simultaneous phenotyping of pectin methylesterases, pectinases, and oligogalacturonides in plants during biotic stresses. Front Plant Sci 6:331

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu G, Ji Y, Bhuiyan NH et al (2010) Amino acid homeostasis modulates salicylic acid-associated redox status and defense responses in Arabidopsis. Plant Cell 22:3845–3863

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu X, Grabherr HM, Willmann R et al (2014) Host-induced bacterial cell wall decomposition mediates pattern-triggered immunity in Arabidopsis. Elife 3:e01990

    PubMed Central  Google Scholar 

  • Liu Z, Yan JP, Li DK et al (2015) UDP-glucosyltransferase71c5, a major glucosyltransferase, mediates abscisic acid homeostasis in Arabidopsis. Plant Physiol 167:1659–1670

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Marco F, Busó E, Carrasco P (2014) Overexpression of SAMDC1 gene in Arabidopsis thaliana increases expression of defense-related genes as well as resistance to Pseudomonas syringae and Hyaloperonospora arabidopsis. Front Plant Sci 5:115

    Article  PubMed  PubMed Central  Google Scholar 

  • Marina M, Sirera FV, Rambla JL et al (2013) Thermospermine catabolism increases Arabidopsis thaliana resistance to Pseudomonas viridiflava. J Exp Bot 64:1393–1402

    Article  CAS  PubMed  Google Scholar 

  • Meschke H, Walter S, Schrempf H (2012) Characterization and localization of prodiginines from Streptomyces lividans suppressing Verticillium dahliae in the absence or presence of Arabidopsis thaliana. Environ Microbiol 14:940–952

    Article  CAS  PubMed  Google Scholar 

  • Meuwly P, Métraux JP (1993) Ortho-anisic acid as internal standard for the simultaneous quantitation of salicylic acid and its putative biosynthetic precursors in cucumber leaves. Anal Biochem 214:500–505

    Article  CAS  PubMed  Google Scholar 

  • Miao W, Wang X, Li M et al (2010) Genetic transformation of cotton with a harpin-encoding gene hpaXoo confers an enhanced defense response against different pathogens through a priming mechanism. BMC Plant Biol 10:67

    Article  PubMed  PubMed Central  Google Scholar 

  • Mo HJ, Wang XF, Zhang Y et al (2015a) Cotton ACAULIS5 is involved in stem elongation and the plant defense response to Verticillium dahliae through thermospermine alteration. Plant Cell Rep 34:1975–1985

    Article  CAS  PubMed  Google Scholar 

  • Mo HJ, Wang XF, Zhang Y et al (2015b) Cotton polyamine oxidase is required for spermine and camalexin signalling in the defence response to Verticillium dahliae. Plant J 83:962–975

    Article  CAS  PubMed  Google Scholar 

  • Momtaz OA, Hussein EM, Fahmy EM et al (2010) Expression of S-adenosyl methionine decarboxylase gene for polyamine accumulation in Egyptian cotton Giza 88 and Giza 90. GM Crops 1:257–266

    Article  PubMed  Google Scholar 

  • Moschou PN, Paschalidis KA, Delis ID et al (2008) Spermidine exodus and oxidation in the apoplast induced by abiotic stress is responsible for H2O2 signatures that direct tolerance responses in tobacco. Plant Cell 20:1708–1724

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nambeesan S, AbuQamar S, Laluk K et al (2012) Polyamines attenuate ethylene-mediated defense responses to abrogate resistance to Botrytis cinerea in tomato. Plant Physiol 158:1034–1045

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prince DC, Drurey C, Zipfel C et al (2014) The leucine-rich repeat receptor-like kinase BRASSINOSTEROID INSENSITIVE1-ASSOCIATED KINASE1 and the cytochrome P450 PHYTOALEXIN DEFICIENT3 contribute to innate immunity to aphids in Arabidopsis. Plant Physiol 164:2207–2219

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raiola A, Lionetti V, Elmaghraby I et al (2011) Pectin methylesterase is induced in Arabidopsis upon infection and is necessary for a successful colonization by necrotrophic pathogens. Mol Plant Microbe In 24:432–440

    Article  CAS  Google Scholar 

  • Ralhan A, Schöttle S, Thurow C et al (2012) The vascular pathogen Verticillium longisporum requires a jasmonic acid-independent COI1 function in roots to elicit disease symptoms in Arabidopsis shoots. Plant Physiol 159:1192–1203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roux M, Schwessinger B, Albrecht C et al (2011) The Arabidopsis leucine-rich repeat receptor-like kinases BAK1/SERK3 and BKK1/SERK4 are required for innate immunity to hemibiotrophic and biotrophic pathogens. Plant Cell 23:2440–2455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sagor GH, Berberich T, Takahashi Y et al (2013) The polyamine spermine protects Arabidopsis from heat stress-induced damage by increasing expression of heat shock-related genes. Transgenic Res 22:595–605

    Article  CAS  PubMed  Google Scholar 

  • Shi H, Chan Z (2014) Improvement of plant abiotic stress tolerance through modulation of the polyamine pathway. J Integr Plant Biol 56:114–121

    Article  CAS  PubMed  Google Scholar 

  • Shi H, Ye T, Zhong B et al (2014) Comparative proteomic and metabolomic analyses reveal mechanisms of improved cold stress tolerance in bermudagrass (Cynodon dactylon (L). Pers.) by exogenous calcium. J Integr Plant Biol 56:1064–1079

    Article  CAS  PubMed  Google Scholar 

  • Sønderby IE, Geu-Flores F, Halkier BA (2010) Biosynthesis of glucosinolates—gene discovery and beyond. Trends Plant Sci 15:283–290

    Article  PubMed  Google Scholar 

  • Song JT, Lu H, Greenberg JT (2004) Divergent roles in Arabidopsis thaliana development and defense of two homologous genes, aberrant growth and death2 and AGD2-LIKE DEFENSE RESPONSE PROTEIN1, encoding novel aminotransferases. Plant Cell 16:353–366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Staswick PE, Tiryaki I (2004) The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis. Plant Cell 16:2117–2127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takahashi Y, Uehara Y, Berberich T et al (2004) A subset of hypersensitive response marker genes, including HSR203J, is the downstream target of a spermine signal transduction pathway in tobacco. Plant J 40:586–595

    Article  CAS  PubMed  Google Scholar 

  • Vernooij B, Friedrich L, Morse A et al (1994) Salicylic acid is not the translocated signal responsible for inducing systemic acquired resistance but is required in signal transduction. Plant Cell 6:959–965

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vlot AC, Dempsey DA, Klessig DF (2009) Salicylic acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol 47:177–206

    Article  CAS  PubMed  Google Scholar 

  • von Saint Paul V, Zhang W, Kanawati B et al (2011) The Arabidopsis glucosyltransferase UGT76B1 conjugates isoleucic acid and modulates plant defense and senescence. Plant Cell 23:4124–4145

    Article  Google Scholar 

  • Walters DR (2003) Polyamines and plant disease. Phytochemistry 64:97–107

    Article  CAS  PubMed  Google Scholar 

  • Xu SL, Rahman A, Baskin TI et al (2008) Two leucine-rich repeat receptor kinases mediate signaling, linking cell wall biosynthesis and ACC synthase in Arabidopsis. Plant Cell 20:3065–3079

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yadeta KA, Hanemian M, Smit P et al (2011) The Arabidopsis thaliana DNA-binding protein AHL19 mediates Verticillium wilt resistance. Mol Plant Microbe In 24:1582–1591

    Article  CAS  Google Scholar 

  • Zeier J (2013) New insights into the regulation of plant immunity by amino acid metabolic pathways. Plant Cell Environ 36:2085–2103

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Wang XF, Yang S et al (2011a) Cloning and characterization of a Verticillium wilt resistance gene from Gossypium barbadense and functional analysis in Arabidopsis thaliana. Plant Cell Rep 30:2085–2096

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z, Chen H, Huang X et al (2011b) BSCTV C2 attenuates the degradation of SAMDC1 to suppress DNA methylation-mediated gene silencing in Arabidopsis. Plant Cell 23:273–288

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We are grateful to Dr Dai Xiao-Feng of the Chinese Academy of Agricultural Sciences for kindly offering V. dahliae strain Vd-GFP-77. We thank Yule Liu of Tsinghua University for graciously providing the TRV vector. This study was supported by funds for the 863 Project (No. 2013AA102601) and the Early-stage Basic Research Key Project of China (No. 2011CB111609).

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    Authors and Affiliations

    1. North China Key Laboratory for Germplasm Resources of Education Ministry, Hebei Agricultural University, Baoding, 071001, China

      Hui-Juan Mo, Xiao-Li Zhu, Xing-Fen Wang, Yan Zhang, Jun Yang, Gui-Jun Yan & Zhi-Ying Ma

    2. Institute of Genetics and Breeding, Langfang Teachers University, Langfang, 065000, China

      Yan-Xiang Sun

    3. School of Plant Biology, Faculty of Science and The UWA Institute of Agriculture, The University of Western Australia, Perth, 6009, Australia

      Gui-Jun Yan

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    1. Hui-Juan Mo
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    H. -J. Mo and Y. -X. Sun contributed equally to this work.

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    425_2015_2463_MOESM1_ESM.docx

    Supplementary Table S1. Levels of amino acids in wild-type, GhSPMS-, and GhSAMDC-overexpressing plants infected with V. dahliae. Values are mean ± SE of three biological replicates from three independent experiments. Asterisks indicate significant differences from mock control (wild-type) (Tukey’s test; *P < 0.05). WT, wild-type (DOCX 61 kb)

    425_2015_2463_MOESM2_ESM.docx

    Supplementary Fig. S1. Amplifications of GhSPMS or GhSAMDC from Arabidopsis genomic DNA (a, b) and cDNA (c, d), respectively. a, b Identification of independent and homozygous T4 lines by PCR using genomic DNA as the templates. AtUBQ5 was used as the internal control. The template of WT (wild-type) was used as the negative control. c, d The relative expression of GhSPMS or GhSAMDC in their five independent and homozygous T4 lines. Transcript levels were determined by real-time RT-PCR, using AtUBQ5 as internal control. The expression of GhSPMS or GhSAMDC was not detected in wild-type plants. Values are mean ± SE of three independent experiments (DOCX 79 kb)

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    Mo, HJ., Sun, YX., Zhu, XL. et al. Cotton S-adenosylmethionine decarboxylase-mediated spermine biosynthesis is required for salicylic acid- and leucine-correlated signaling in the defense response to Verticillium dahliae . Planta 243, 1023–1039 (2016). https://doi.org/10.1007/s00425-015-2463-5

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