Advertisement

Journal of Plant Growth Regulation

, Volume 38, Issue 4, pp 1507–1515 | Cite as

Transcriptomic Profiling of Rice Seedlings Inoculated with the Symbiotic Fungus Trichoderma asperellum SL2

  • Febri DoniEmail author
  • F. Fathurrahman
  • Muhamad Shakirin MispanEmail author
  • Nurul Shamsinah Mohd Suhaimi
  • Wan Mohtar Wan Yusoff
  • Norman Uphoff
Article

Abstract

The fungal species Trichoderma is reported to have a significant impact on the growth and physiological performance of rice plants. However, the molecular mechanisms that induce these effects remain unspecified. Using next-generation sequencing technology, this study compared the differential expression of genes in rice seedlings that had been inoculated with Trichoderma asperellum SL2 with the gene expression in seedlings that had no such inoculation. The study showed that many genes related to plant growth enhancement and physiological functioning are differentially expressed in seedlings which have been symbiotically colonized by T. asperellum SL2. In these seedlings, specific genes related to photosynthesis, RNA activity, stomatal activity, and root development were found to be up-regulated as others were down-regulated. Although the exact causal mechanisms at the molecular level remain to be identified, the presence of Trichoderma versus its absence was associated with almost ten times more significant up-regulations than down-regulations for specific genes that have been identified from previous genomic mapping. Such analysis at the molecular level can help to explain observed phenotypic effects at the organismic level, and it begins to illuminate the observed beneficial relationships expressed phenotypically between crop plants and certain symbiotic microbes.

Keywords

Gene expression Rice Transcriptomic analysis Trichoderma 

Notes

Acknowledgements

We express appreciation for helpful feedback and suggestions from Dr. Gary Harman, Professor Emeritus, Cornell University, Geneva, NY, USA.

Compliance with Ethical Standards

Conflict of interest

The authors declare no conflicts of interest.

References

  1. Alhasnawi AN, Radziah CC, Kadhimi AA, Isahak A, Mohamad A, Yusoff WM (2017) Relationship observed between salinity-tolerant callus cell lines and anatomical structure of Line 2 (Oryza sativa L.) indica under salinity stress. Biocatal Agric Biotechnol 10:367–378Google Scholar
  2. Azad K, Kaminskyj S (2016) A fungal endophyte strategy for mitigating the effect of salt and drought stress on plant growth. Symbiosis 68:73–78Google Scholar
  3. Bae H, Sicher RC, Kim MS, Kim SH, Strem MD, Melnick RL, Bailey BA (2009) The beneficial endophyte Trichoderma hamatum isolate DIS 219b promotes growth and delays the onset of the drought response in Theobroma cacao. J Exp Bot 60:3279–3295PubMedPubMedCentralGoogle Scholar
  4. Bailey BA, Bae H, Strem MD, Roberts DP, Thomas SE, Crozier J, Samuels GJ, Choi IY, Holmes KA (2006) Fungal and plant gene expression during the colonization of cacao seedlings by endophytic isolates of four Trichoderma species. Planta 224:1449–1464PubMedGoogle Scholar
  5. Bharti N, Pandey SS, Barnawal D, Patel VK, Kalra A (2016) Plant growth promoting rhizobacteria Dietzia natronolimnaea modulates the expression of stress responsive genes providing protection of wheat from salinity stress. Sci Rep 6:34768PubMedPubMedCentralGoogle Scholar
  6. Blilou I, Ocampo JA, García-Garrido JM (2000) Induction of Ltp (lipid transfer protein) and Pal (phenylalanine ammonia-lyase) gene expression in rice roots colonized by the arbuscular mycorrhizal fungus Glomus mosseae. J Exp Bot 51:1969–1977PubMedGoogle Scholar
  7. Chacón MR, Rodríguez Galán O, Benítez Fernández CT, Sousa S, Rey M, Llobell González A, Delgado Jarana J (2007) Microscopic and transcriptome analyses of early colonization of tomato roots by Trichoderma harzianum. ‎Int Microbiol 10(1):19–27PubMedGoogle Scholar
  8. Colmer TD, Armstrong W, Greenway H, Ismail AM, Kirk GJD, Atwell BJ (2014) Physiological mechanisms of flooding tolerance in rice: transient complete submergence and prolonged standing water. In: Luttge U, Beyschlag W, Cushman J (eds) Progress in botany, vol 75. Springer, Berlin, pp. 255–307Google Scholar
  9. Contreras-Cornejo HA, Macías-Rodríguez L, Cortés-Penagos C, López-Bucio J (2009) Trichoderma virens, a plant beneficial fungus, enhances biomass production and promotes lateral root growth through an auxin-dependent mechanism in Arabidopsis. Plant Physiol 149:1579–1592PubMedPubMedCentralGoogle Scholar
  10. Contreras-Cornejo HA, Macías-Rodríguez L, Alfaro-Cuevas R, Lopez-Bucio (2014) Trichoderma spp. improve growth of Arabidopsis seedlings under salt stress through enhanced root development, osmolite production, and Na+ elimination through root exudates. Mol Plant Microbe Interact 27(6):503–514PubMedGoogle Scholar
  11. Contreras-Cornejo HA, Macías-Rodríguez L, Vergara AG, López-Bucio J (2015) Trichoderma modulates stomatal aperture and leaf transpiration through an abscisic acid-dependent mechanism in arabidopsis. J Plant Growth Regul 34:425–432Google Scholar
  12. Contreras-Cornejo HA, Macías-Rodríguez L, del-Val E, Larsen J (2018) The root endophytic fungus Trichoderma atroviride induces foliar herbivory resistance in maize plants. Appl Soil Ecol 124:45–53Google Scholar
  13. Doni F (2018) Trichoderma asperellum SL2 for improving growth, gene expression pattern, physiological traits, yield and disease resistance of rice plants under System of Rice Intensification (SRI) management system. PhD thesis, The National University of Malaysia, Bangi, MalaysiaGoogle Scholar
  14. Doni F, Anizan I, Che Radziah CMZ, Wan Mohtar WY (2014) Physiological and growth response of rice (Oryza sativa L.) plants to Trichoderma spp. inoculants. AMB Express 4:45PubMedPubMedCentralGoogle Scholar
  15. Doni F, Che Radziah CMZ, Anizan I, Norela S, Fathurrahman F, Uphoff N, Wan Mohtar WY (2017) Relationships observed between Trichoderma inoculation and characteristics of rice grown under System of Rice Intensification (SRI) vs. conventional methods of cultivation. Symbiosis 72:45–59Google Scholar
  16. Doni F, Zain CR, Isahak A, Fathurrahman F, Anhar A, Mohamad WN, Yusoff WM, Uphoff N (2018) A simple, efficient, and farmer-friendly Trichoderma-based biofertilizer evaluated with the SRI Rice Management System. Org Agric 8:207–223Google Scholar
  17. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930Google Scholar
  18. Guler NS, Pehlivan N, Karaoglu SA, Guzel S, Bozdeveci A (2016) Trichoderma atroviride ID20G inoculation ameliorates drought stress-induced damages by improving antioxidant defence in maize seedlings. Acta Physiol Plant.  https://doi.org/10.1007/s11738-016-2153-3 CrossRefGoogle Scholar
  19. Gunapati S, Naresh R, Ranjan S, Nigam D, Hans A, Verma PC, Gadre R, Pathre UV, Sane AP, Sane VA (2016) Expression of GhNAC2 from G. herbaceum, improves root growth and imparts tolerance to drought in transgenic cotton and Arabidopsis. Sci Rep 6:24978PubMedPubMedCentralGoogle Scholar
  20. Haefele SM, Siopongco JD, Boling AA, Bouman BA, Tuong TP (2009) Transpiration efficiency of rice (Oryza sativa L.). Field Crops Res 111(1):1–10Google Scholar
  21. Harman GE (2011) Multifunctional fungal plant symbionts: New tools to enhance plant growth and productivity. New Phytol 189:647–649PubMedGoogle Scholar
  22. Malinovsky FG, Fangel JU, Willats WG (2014) The role of the cell wall in plant immunity. Front Plant Sci.  https://doi.org/10.3389/fpls.2014.00178 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Maruyama K, Urano K, Yoshiwara K, Morishita Y, Sakurai N, Suzuki H, Kojima M, Sakakibara H, Shibata D, Saito K, Shinozaki K (2014) Integrated analysis of the effects of cold and dehydration on rice metabolites, phytohormones, and gene transcripts. Plant Physiol 164:1759–1771PubMedPubMedCentralGoogle Scholar
  24. Mastouri F, Björkman T, Harman GE (2010) Seed treatment with Trichoderma harzianum alleviates biotic, abiotic, and physiological stresses in germinating seeds and seedlings. Phytopathol 100:1213–1221Google Scholar
  25. Mastouri F, Björkman T, Harman GE (2012) Trichoderma harzianum enhances antioxidant defense of tomato seedlings and resistance to water deficit. Mol Plant Microbe Interact 25:1264–1271PubMedGoogle Scholar
  26. Mishra A, Salokhe VM (2011) Rice root growth and physiological responses to SRI water management and implications for crop productivity. Paddy Water Environ 9:41–52Google Scholar
  27. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trend Plant Sci 9:490–498Google Scholar
  28. Nawrocka J, Malolepsza U (2013) Diversity in plant systemic resistance induced by Trichoderma. Biol Control 67:149–156Google Scholar
  29. Neumann B, Laing M (2006) Trichoderma: an ally in the quest for soil system sustainability. In: Uphoff N, Fernandes E, Herren H, Husson O, Laing M, Palm C, Pretty J, Sanchez P, Sanginga N, Thies J (eds) Biological approaches to sustainable soil systems. CRC Press, Boca Raton, pp 491–500Google Scholar
  30. Nguyen HT, Babu RC, Blum A (1997) Breeding for drought resistance in rice: Physiology and molecular genetics considerations. Crop Sci 37(5):1426–1434Google Scholar
  31. Nicolás C, Hermosa R, Rubio B, Mukherjee PK, Monte E (2014) Trichoderma genes in plants for stress tolerance-status and prospects. Plant Sci 228:71–78PubMedGoogle Scholar
  32. Novogene (2017) Whole genome sequencing. https://en.novogene.com/next-generation-sequencing-services/
  33. Pandey V, Ansari MW, Tula S, Yadav S, Sahoo RK, Shukla N, Bains G, Badal S, Chandra S, Gaur AK, Kumar A (2016) Dose-dependent response of Trichoderma harzianum in improving drought tolerance in rice genotypes. Planta 243:1251–1264PubMedGoogle Scholar
  34. Pascale A, Vinale F, Manganiello G, Nigro M, Lanzuise S, Ruocco M, Marra R, Lombardi N, Woo SL, Lorito M (2017) Trichoderma and its secondary metabolites improve yield and quality of grapes. Crop Prot 92:176–181Google Scholar
  35. Rediers H, Bonnecarrere V, Rainey PB, Hamonts K, Vanderleyden J, De Mot R (2003) Development and application of a dapB-based in vivo expression technology system to study colonization of rice by the endophytic nitrogen-fixing bacterium Pseudomonas stutzeri A15. Appl Environ Microbiol 69:6864–6874PubMedPubMedCentralGoogle Scholar
  36. Redman RS, Kim YO, Woodward CJ, Greer C, Espino L, Doty SL, Rodriguez RJ (2011) Increased fitness of rice plants to abiotic stress via habitat adapted symbiosis: a strategy for mitigating impacts of climate change. PLoS ONE 6(7):e14823PubMedPubMedCentralGoogle Scholar
  37. Rodriguez R, Redman R (2005) Balancing the generation and elimination of reactive oxygen species. Proc Natl Acad Sci USA 102:3175–3176PubMedGoogle Scholar
  38. Rodriguez RJ, White JF Jr, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330Google Scholar
  39. Rodriguez RJ, Henson J, Van Volkenburgh E, Hoy M, Wright L, Beckwith F, Kim YO, Redman RS (2008) Stress tolerance in plants via habitat-adapted symbiosis. ISME J 2(4):404–416Google Scholar
  40. Samolski I, Rincón AM, Pinzón LM, Viterbo A, Monte E (2012) The qid74 gene from Trichoderma harzianum has a role in root architecture and plant biofertilization. Microbiology 158(1):129–138PubMedGoogle Scholar
  41. Segarra G, Casanova E, Bellido D, Odena MA, Oliveira E, Trillas I (2007) Proteome, salicylic acid, and jasmonic acid changes in cucumber plants inoculated with Trichoderma asperellum strain T34. Proteomics 7:3943–3952PubMedGoogle Scholar
  42. Shoresh M, Harman GE (2008a) The relationship between increased growth and resistance induced in plants by root colonizing microbes. Plant Signal Behav 3:737–739PubMedPubMedCentralGoogle Scholar
  43. Shoresh M, Harman GE (2008b) The molecular basis of shoot responses of maize seedlings to Trichoderma harzianum T22 inoculation of the root: a proteomic approach. Plant Physiol 147:2147–2163PubMedPubMedCentralGoogle Scholar
  44. Shoresh M, Yedidia I, Chet I (2005) Involvement of jasmonic acid/ethylene signaling pathway in the systemic resistance induced in cucumber by Trichoderma asperellum T203. Phytopathol 95:76–84Google Scholar
  45. Shoresh M, Harman GE, Mastouri F (2010) Induced systemic resistance and plant responses to fungal biocontrol agents. Annu Rev of Phytopathol 48:21–43Google Scholar
  46. Shukla N, Awasthi RP, Rawat L, Kumar J (2012) Biochemical and physiological responses of rice (Oryza sativa L.) as influenced by Trichoderma harzianum under drought stress. Plant Physiol Biochem 54:78–88PubMedGoogle Scholar
  47. Srivastava S, Chaudhry V, Mishra A, Chauhan PS, Rehman A, Yadav A, Tuteja N, Nautiyal CS (2012) Gene expression profiling through microarray analysis in Arabidopsis thaliana colonized by Pseudomonas putida MTCC5279, a plant growth promoting rhizobacterium. Plant Signal Behav 7:235–245PubMedPubMedCentralGoogle Scholar
  48. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511–515PubMedPubMedCentralGoogle Scholar
  49. Underwood D (2012) The plant cell wall: a dynamic barrier against pathogen invasion. Front Plant Sci 3:1–6Google Scholar
  50. Vargas WA, Crutcher FK, Kenerley CM (2011) Functional characterization of a plant-like sucrose transporter from the beneficial fungus Trichoderma virens: Regulation of the symbiotic association with plants by sucrose metabolism inside the fungal cells. New Phytol 189:777–789PubMedGoogle Scholar
  51. Varshney RK, Nayak SN, May GD, Jackson SA (2009) Next-generation sequencing technologies and their implications for crop genetics and breeding. Trends Biotechnol 27:522–530PubMedGoogle Scholar
  52. Viterbo A, Landau U, Kim S, Chernin L, Chet I (2010) Characterization of ACC deaminase from the biocontrol and plant growth-promoting agent Trichoderma asperellum T203. FEMS Microbiol Lett 305:42–48PubMedGoogle Scholar
  53. Wani ZA, Ashraf N, Mohiuddin T, Riyaz-Ul-Hassan S (2015) Plant-endophyte symbiosis, an ecological perspective. Appl Microbiol Biotechnol 99:2955–2965PubMedGoogle Scholar
  54. Wu Q, Peng X, Yang M, Zhang W, Dazzo FB, Uphoff N, Jing Y, Shen S (2018) Rhizobia promote the growth of rice shoots by targeting cell signaling, division and expansion. Plant Mol Biol 97:507–523PubMedGoogle Scholar
  55. Yedidia I, Srivastva AK, Kapulnik Y, Chet I (2001) Effect of Trichoderma harzianum on microelement concentrations and increased growth of cucumber plants. Plant Soil 235:235–242Google Scholar
  56. Zaidi NW, Singh M, Kumar S, Sangle UR, Singh R, Prasad R, Singh SS, Singh S, Yadav AK, Singh A, Waza SA (2018) Trichoderma harzianum improves the performance of stress-tolerant rice varieties in rainfed ecologies of Bihar, India. Field Crops Res 220:97–104Google Scholar
  57. Zipfel C, Oldroyd GE (2017) Plant signaling in symbiosis and immunity. Nature 543:328PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Institute of Biological Sciences, Faculty of ScienceUniversity of MalayaKuala LumpurMalaysia
  2. 2.Department of Agrotechnology, Faculty of AgricultureUniversitas Islam RiauPekanbaruIndonesia
  3. 3.Centre for Research in Biotechnology for AgricultureUniversity of MalayaKuala LumpurMalaysia
  4. 4.School of Biosciences and Biotechnology, Faculty of Science and TechnologyUniversiti Kebangsaan MalaysiaBangiMalaysia
  5. 5.SRI International Network and Resources CenterCornell UniversityIthacaUSA

Personalised recommendations