Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Crop and Pasture Science Crop and Pasture Science Society
Plant sciences, sustainable farming systems and food quality
RESEARCH ARTICLE

Functional analysis of the soybean gene GmTIR under biotic and abiotic stresses

Xiaoting Wang A , Lu Huang A , Xiaochun Bian A , Zhan Li A , Ruifang Gao A , Xing Zhang A , Xiaoli Zhang A , Xiangnan Li A , Haitang Wang A , Na Guo A , Jianying Feng A , Jinming Zhao A B and Han Xing https://orcid.org/0000-0003-3200-2572 A B
+ Author Affiliations
- Author Affiliations

A Soybean Research Institute, National Center for Soybean Improvement, Key Laboratory of Biology and Genetic Improvement of Soybean (General, Ministry of Agriculture), State Key Laboratory of Crop Genetics and Germplasm Enhancement, Jiangsu Collaborative Innovation Center for Modern Crop Production, Nanjing Agricultural University, Nanjing, Jiangsu 210095, China.

B Corresponding authors. Email: jmz3000@126.com; hanx@njau.edu.cn

Crop and Pasture Science 71(1) 47-55 https://doi.org/10.1071/CP19219
Submitted: 29 May 2019  Accepted: 3 September 2019   Published: 3 February 2020

Abstract

The TIR (Toll/interleukin-1 receptor) domain has been proposed to play a signalling role in resistance responses mediated by TIR-containing proteins. The functions of some TIR-domain-containing proteins have been defined in some plants; however, there has been no study evaluating TIR-domain-containing proteins in soybean (Glycine max (L.) Merr.). In this study, GmTIR was isolated from soybean, and its functions under stresses were analysed. Analysis of tissue-specific expression patterns showed that GmTIR was strongly expressed in leaves and weakly expressed in the immature green beans. Treatments with Phytophthora sojae, salicylic acid, methyl jasmonate, abscisic acid, copper, salt and drought significantly increased GmTIR expression, and 1-aminocyclopropane-1-carboxylic acid and low temperature caused slight increases. Compared with wild type expression, GmTIR overexpression in Arabidopsis thaliana led to a higher germination rate under both salt and drought stresses, but the root length of transgenic Arabidopsis was greater than of wild type plants only under salt stress. In response to the stresses, accumulation of proline in transgenic plants was also higher. The results suggest that GmTIR could be a positive factor for promoting the survival of plants under biotic and abiotic stresses.

Additional keywords: ABA, phenotype, osmotic substance, sequence analysis, transgenic hormone.


References

American Soybean Association (2016) ‘SoyStats: a reference guide to soybean facts and figures.’ (American Soybean Association: St. Louis, MO, USA) http://www.soystats.com

Anderson PA, Lawrence GJ, Morrish BC, Ayliffe MA, Finnegan EJ, Ellis JG (1997) Inactivation of the flax rust resistance gene M associated with loss of a repeated unit within the leucine-rich repeat coding region. The Plant Cell 9, 641–651.

Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796
Analysis of the genome sequence of the flowering plant Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 11130711PubMed |

Audenaert K, De Meyer GB, Höfte MM (2002) Abscisic acid determines basal susceptibility of tomato to Botrytis cinerea and suppresses salicylic acid-dependent signaling mechanisms. Plant Physiology 128, 491–501.
Abscisic acid determines basal susceptibility of tomato to Botrytis cinerea and suppresses salicylic acid-dependent signaling mechanisms.Crossref | GoogleScholarGoogle Scholar | 11842153PubMed |

Bernoux M, Ve T, Williams S, Warren C, Hatters D, Valkov E, Zhang X, Ellis JG, Kobe B, Dodds PN (2011) Structural and functional analysis of a plant resistance protein TIR domain reveals interfaces for self-association, signaling, and autoregulation. Cell Host & Microbe 9, 200–211.
Structural and functional analysis of a plant resistance protein TIR domain reveals interfaces for self-association, signaling, and autoregulation.Crossref | GoogleScholarGoogle Scholar |

Botella MA, Parker JE, Frost LN, Bittner-Eddy PD, Beynon JL, Daniels MJ, Holub EB, Jones JD (1998) Three genes of the Arabidopsis RPP1 complex resistance locus recognize distinct Peronospora parasitica avirulence determinants. The Plant Cell 10, 1847–1860.
Three genes of the Arabidopsis RPP1 complex resistance locus recognize distinct Peronospora parasitica avirulence determinants.Crossref | GoogleScholarGoogle Scholar | 9811793PubMed |

Chang RZ, Chen YW, Shao GH, Wan CW (1994) Effect of salt on agricultural characters and chemical quality of seed in soybeans. Dadou Kexue 13, 101–105.

Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium‐mediated transformation of Arabidopsis thaliana. The Plant Journal 16, 735–743.
Floral dip: a simplified method for Agrobacterium‐mediated transformation of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 10069079PubMed |

Cui X, Yan Q, Gan S, Xue D, Dou D, Guo N, Xing H (2017) Overexpression of gma-miR1510a/b suppresses the expression of a NB-LRR domain gene and reduces resistance to Phytophthora sojae. Gene 621, 32–39.
Overexpression of gma-miR1510a/b suppresses the expression of a NB-LRR domain gene and reduces resistance to Phytophthora sojae.Crossref | GoogleScholarGoogle Scholar | 28411083PubMed |

Di X, Gomila J, Takken FL (2017) Involvement of salicylic acid, ethylene and jasmonic acid signalling pathways in the susceptibility of tomato to Fusarium oxysporum. Molecular Plant Pathology 18, 1024–1035.
Involvement of salicylic acid, ethylene and jasmonic acid signalling pathways in the susceptibility of tomato to Fusarium oxysporum.Crossref | GoogleScholarGoogle Scholar | 28390170PubMed |

Dinesh-Kumar SP, Tham WH, Baker BJ (2000) Structure-function analysis of the tobacco mosaic virus resistance gene N. Proceedings of the National Academy of Sciences of the United States of America 97, 14789–14794.
Structure-function analysis of the tobacco mosaic virus resistance gene N.Crossref | GoogleScholarGoogle Scholar | 11121079PubMed |

Feechan A, Anderson C, Torregrosa L, Jermakow A, Mestre P, Wiedemann-Merdinoglu S, Merdinoglu D, Walker AR, Cadle-Davidson L, Reisch B, Aubourg S, Bentahar N, Shrestha B, Bouquet A, Adam-Blondon AF, Thomas MR, Dry IB (2013) Genetic dissection of a TIR-NB-LRR locus from the wild North American grapevine species Muscadinia rotundifolia identifies paralogous genes conferring resistance to major fungal and oomycete pathogens in cultivated grapevine. The Plant Journal 76, 661–674.
Genetic dissection of a TIR-NB-LRR locus from the wild North American grapevine species Muscadinia rotundifolia identifies paralogous genes conferring resistance to major fungal and oomycete pathogens in cultivated grapevine.Crossref | GoogleScholarGoogle Scholar | 24033846PubMed |

Finkelstein RR, Gibson SI (2002) ABA and sugar interactions regulating development: cross-talk or voices in a crowd? Current Opinion in Plant Biology 5, 26–32.
ABA and sugar interactions regulating development: cross-talk or voices in a crowd?Crossref | GoogleScholarGoogle Scholar | 11788304PubMed |

Gassmann W, Hinsch ME, Staskawicz BJ (1999) The Arabidopsis RPS4 bacterial‐resistance gene is a member of the TIR‐NBS‐LRR family of disease‐resistance genes. The Plant Journal 20, 265–277.
The Arabidopsis RPS4 bacterial‐resistance gene is a member of the TIR‐NBS‐LRR family of disease‐resistance genes.Crossref | GoogleScholarGoogle Scholar | 10571887PubMed |

Gay NJ, Gangloff M (2007) Structure and function of Toll receptors and their ligands. Annual Review of Biochemistry 76, 141–165.
Structure and function of Toll receptors and their ligands.Crossref | GoogleScholarGoogle Scholar | 17362201PubMed |

Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A (2012) Role of proline under changing environments. Plant Signaling & Behavior 7, 1456–1466.
Role of proline under changing environments.Crossref | GoogleScholarGoogle Scholar |

Hoque MA, Banu MN, Nakamura Y, Shimoishi Y, Murata Y (2008) Proline and glycinebetaine enhance antioxidant defense and methylglyoxal detoxification systems and reduce NaCl-induced damage in cultured tobacco cells. Journal of Plant Physiology 165, 813–824.
Proline and glycinebetaine enhance antioxidant defense and methylglyoxal detoxification systems and reduce NaCl-induced damage in cultured tobacco cells.Crossref | GoogleScholarGoogle Scholar | 17920727PubMed |

Hu CA, Delauney AJ, Verma DP (1992) A bifunctional enzyme (delta 1-pyrroline-5-carboxylate synthetase) catalyzes the first two steps in proline biosynthesis in plants. Proceedings of the National Academy of Sciences of the United States of America 89, 9354–9358.
A bifunctional enzyme (delta 1-pyrroline-5-carboxylate synthetase) catalyzes the first two steps in proline biosynthesis in plants.Crossref | GoogleScholarGoogle Scholar | 1384052PubMed |

Khan MS, Khan MA, Ahmad D (2016) Assessing utilization and environmental risks of important genes in plant abiotic stress tolerance. Frontiers in Plant Science 7, 792
Assessing utilization and environmental risks of important genes in plant abiotic stress tolerance.Crossref | GoogleScholarGoogle Scholar | 27446095PubMed |

Ku Y, Sintaha M, Cheung M, Lam H (2018) Plant hormone signaling crosstalks between biotic and abiotic stress responses. International Journal of Molecular Sciences 19, 3206
Plant hormone signaling crosstalks between biotic and abiotic stress responses.Crossref | GoogleScholarGoogle Scholar |

Kumar H, Kawai T, Akira S (2009) Pathogen recognition in the innate immune response. The Biochemical Journal 420, 1–16.
Pathogen recognition in the innate immune response.Crossref | GoogleScholarGoogle Scholar | 19382893PubMed |

Lawrence GJ, Finnegan EJ, Ayliffe MA, Ellis JG (1995) The L6 gene for flax rust resistance is related to the Arabidopsis bacterial resistance gene RPS2 and the tobacco viral resistance gene N. The Plant Cell 7, 1195–1206.

Li XL, Zhang YL, Yin L, Lu J (2017) Overexpression of pathogen-induced grapevine TIR-NB-LRR gene VaRGA1 enhances disease resistance and drought and salt tolerance in Nicotiana benthamiana. Protoplasma 254, 957–969.
Overexpression of pathogen-induced grapevine TIR-NB-LRR gene VaRGA1 enhances disease resistance and drought and salt tolerance in Nicotiana benthamiana.Crossref | GoogleScholarGoogle Scholar |

Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method. Methods 25, 402–408.
Analysis of relative gene expression data using real-time quantitative PCR and the 2ΔΔCT method.Crossref | GoogleScholarGoogle Scholar | 11846609PubMed |

Manavalan LP, Guttikonda SK, Tran LS, Nguyen HT (2009) Physiological and molecular approaches to improve drought resistance in soybean. Plant Cell Physiology 50, 1260–1276.
Physiological and molecular approaches to improve drought resistance in soybean.Crossref | GoogleScholarGoogle Scholar | 19546148PubMed |

Mauch-Mani B, Mauch F (2005) The role of abscisic acid in plant-pathogen interactions. Current Opinion in Plant Biology 8, 409–414.

Müller M, Munné-Bosch S (2015) Ethylene response factors: a key regulatory hub in hormone and stress signaling. Plant Physiology 169, 32–41.
Ethylene response factors: a key regulatory hub in hormone and stress signaling.Crossref | GoogleScholarGoogle Scholar | 26103991PubMed |

Nüsslein-Volhard C, Wieschaus E (1980) Mutations affecting segment number and polarity in Drosophila. Nature 287, 795
Mutations affecting segment number and polarity in Drosophila.Crossref | GoogleScholarGoogle Scholar | 6776413PubMed |

Parker JE, Coleman MJ, Szabò V, Frost LN, Schmidt R, van der Biezen EA, Moores T, Dean C, Daniels MJ, Jones JD (1997) The Arabidopsis downy mildew resistance gene RPP5 shares similarity to the toll and interleukin-1 receptors with N and L6. The Plant Cell 9, 879–894.
The Arabidopsis downy mildew resistance gene RPP5 shares similarity to the toll and interleukin-1 receptors with N and L6.Crossref | GoogleScholarGoogle Scholar | 9212464PubMed |

Phang TH, Shao GH, Lam HM (2008) Salt tolerance in soybean. Journal of Integrative Plant Biology 50, 1196–1212.
Salt tolerance in soybean.Crossref | GoogleScholarGoogle Scholar | 19017107PubMed |

Radons J, Falk W, Dove S (2015) Identification of critical regions within the TIR domain of IL-1 receptor type I. The International Journal of Biochemistry & Cell Biology 68, 15–20.
Identification of critical regions within the TIR domain of IL-1 receptor type I.Crossref | GoogleScholarGoogle Scholar |

Rentsch D, Hirner B, Schmelzer E, Frommer WB (1996) Salt stress-induced proline transporters and salt stress-repressed broad specificity amino acid permeases identified by suppression of a yeast amino acid permease-targeting mutant. The Plant Cell 8, 1437–1446.

Ruan CJ, Teixeira da Silva JAT (2011) Metabolomics: creating new potentials for unraveling the mechanisms in response to salt and drought stress and for the biotechnological improvement of xero-halophytes. Critical Reviews in Biotechnology 31, 153–169.
Metabolomics: creating new potentials for unraveling the mechanisms in response to salt and drought stress and for the biotechnological improvement of xero-halophytes.Crossref | GoogleScholarGoogle Scholar | 21058928PubMed |

Ryu CM, Murphy JF, Mysore KS, Kloepper JW (2004) Plant growth-promoting rhizobacteria systemically protect Arabidopsis thaliana against Cucumber mosaic virus by a salicylic acid and NPR1‐independent and jasmonic acid‐dependent signaling pathway. The Plant Journal 39, 381–392.
Plant growth-promoting rhizobacteria systemically protect Arabidopsis thaliana against Cucumber mosaic virus by a salicylic acid and NPR1‐independent and jasmonic acid‐dependent signaling pathway.Crossref | GoogleScholarGoogle Scholar | 15255867PubMed |

Sarazin V, Duclercq J, Mendou B, Aubanelle L, Nicolas V, Aono M, Pilard S, Guerineau F, Sangwan-Norreel B, Sangwan RS (2015) Arabidopsis BNT1, an atypical TIR-NBS-LRR gene, acting as a regulator of the hormonal response to stress. Plant Science 239, 216–229.
Arabidopsis BNT1, an atypical TIR-NBS-LRR gene, acting as a regulator of the hormonal response to stress.Crossref | GoogleScholarGoogle Scholar | 26398806PubMed |

Silveira JA, Viégas Rde A, da Rocha IM, Moreira AC, Moreira Rde A, Oliveira JT (2003) Proline accumulation and glutamine synthetase activity are increased by salt-induced proteolysis in cashew leaves. Journal of Plant Physiology 160, 115–123.
Proline accumulation and glutamine synthetase activity are increased by salt-induced proteolysis in cashew leaves.Crossref | GoogleScholarGoogle Scholar | 12685027PubMed |

Sugano S, Sugimoto T, Takatsuji H, Jiang C (2013) Induction of resistance to Phytophthora sojae in soyabean (Glycine max) by salicylic acid and ethylene. Plant Pathology 62, 1048–1056.
Induction of resistance to Phytophthora sojae in soyabean (Glycine max) by salicylic acid and ethylene.Crossref | GoogleScholarGoogle Scholar |

Sun S, Wu XL, Zhao JM, Wang YC, Tang QH (2011) Characterization and mapping of RpsYu25, a novel resistance gene to Phytophthora sojae. Plant Breeding 130, 139–143.
Characterization and mapping of RpsYu25, a novel resistance gene to Phytophthora sojae.Crossref | GoogleScholarGoogle Scholar |

Sun JT, Li LH, Zhao JM, Huang J, Yan Q, Xing H, Guo N (2014) Genetic analysis and fine mapping of RpsJS, a novel resistance gene to Phytophthora sojae in soybean [Glycine max (L.) Merr.]. Theoretical and Applied Genetics 127, 913–919.
Genetic analysis and fine mapping of RpsJS, a novel resistance gene to Phytophthora sojae in soybean [Glycine max (L.) Merr.].Crossref | GoogleScholarGoogle Scholar |

Ton J, Flors V, Mauch-Mani B (2009) The multifaceted role of ABA in disease resistance. Trends in Plant Science 14, 310–317.
The multifaceted role of ABA in disease resistance.Crossref | GoogleScholarGoogle Scholar | 19443266PubMed |

Ve T, Williams SJ, Kobe B (2015) Structure and function of Toll/interleukin-1 receptor/resistance protein (TIR) domains. Apoptosis 20, 250–261.
Structure and function of Toll/interleukin-1 receptor/resistance protein (TIR) domains.Crossref | GoogleScholarGoogle Scholar | 25451009PubMed |

Wang ZQ, Yuan YZ, Ou JQ, Lin QH, Zhang CF (2007) Glutamine synthetase and glutamate dehydrogenase contribute differentially to proline accumulation in leaves of wheat (Triticum aestivum) seedlings exposed to different salinity. Journal of Plant Physiology 164, 695–701.
Glutamine synthetase and glutamate dehydrogenase contribute differentially to proline accumulation in leaves of wheat (Triticum aestivum) seedlings exposed to different salinity.Crossref | GoogleScholarGoogle Scholar | 16777263PubMed |

Weaver LM, Swiderski MR, Li Y, Jones JD (2006) The Arabidopsis thaliana TIR-NB-LRR R-protein, RPP1A; protein localization and constitutive activation of defence by truncated alleles in tobacco and Arabidopsis. The Plant Journal 47, 829–840.
The Arabidopsis thaliana TIR-NB-LRR R-protein, RPP1A; protein localization and constitutive activation of defence by truncated alleles in tobacco and Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Whitham S, Dinesh-Kumar SP, Choi D, Hehl R, Corr C, Baker B (1994) The product of the tobacco mosaic virus resistance gene N: similarity to toll and the interleukin-1 receptor. Cell 78, 1101–1115.
The product of the tobacco mosaic virus resistance gene N: similarity to toll and the interleukin-1 receptor.Crossref | GoogleScholarGoogle Scholar | 7923359PubMed |

Yang Y, Guo Y (2018) Unraveling salt stress signaling in plants. Journal of Integrative Plant Biology 60, 796–804.
Unraveling salt stress signaling in plants.Crossref | GoogleScholarGoogle Scholar | 29905393PubMed |

Yruela I (2005) Copper in plants. Brazilian Journal of Plant Physiology 17, 145–156.
Copper in plants.Crossref | GoogleScholarGoogle Scholar |

Yuan M, Huang Y, Ge W, Jia Z, Song S, Zhang L, Huang Y (2019) Involvement of jasmonic acid, ethylene and salicylic acid signaling pathways behind the systemic resistance induced by Trichoderma longibrachiatum H9 in cucumber. BMC Genomics 20, 144
Involvement of jasmonic acid, ethylene and salicylic acid signaling pathways behind the systemic resistance induced by Trichoderma longibrachiatum H9 in cucumber.Crossref | GoogleScholarGoogle Scholar | 30777003PubMed |