Symbiosis

, Volume 72, Issue 1, pp 45–59 | Cite as

Relationships observed between Trichoderma inoculation and characteristics of rice grown under System of Rice Intensification (SRI) vs. conventional methods of cultivation

  • Febri Doni
  • Che Radziah Che Mohd Zain
  • Anizan Isahak
  • F. Fathurrahman
  • Norela Sulaiman
  • Norman Uphoff
  • Wan Mohtar Wan Yusoff
Article

Abstract

The System of Rice Intensification (SRI), a management-based approach for improving rice production, has demonstrated various positive effects on rice plants’ growth, resilience and yield. These effects have been attributed in part to symbiotic interactions between rice plants and the microbes that live around, on and inside them; but research on this is still very limited. To examine such relationships, a multifunctional symbiotic fungus Trichoderma asperellum SL2 was evaluated to assess its effects, if any, on the germination and growth of young seedlings and then the subsequent performance of rice plants during their crop cycle. Greenhouse studies were conducted under gnotobiotic conditions to assess any effects associated with inoculating rice seeds with Trichoderma asperellum SL2 compared with uninoculated controls in terms of seedling establishment, an essential part of SRI methodology; and then assessing the capacity of this fungus to enhance the growth, physiological characteristics, nutrient uptake, and yield of rice plants growing under simulated SRI conditions. Results showed that the presence of Trichoderma asperellum SL2 in association with SRI cultural practices led to significant increases in rice seedling growth, germination rate, vigour index, and chlorophyll content, and elicited more favourable phenotypical responses from given genotype potential. The research observations further illustrated that for some parameters, there were no significant differences between inoculated and uninoculated SRI plants, both giving results superior to those for conventionally-grown plants even when inoculated. This indicated that SRI growing conditions are more favorable for Trichoderma to contribute towards the growth, physiological traits, nutrient uptake, and yield of plants, whereas conventional management methods diminish or inhibit these effects. Focused research remains to be done to establish how aerobic microbes such as Trichoderma can affect and accelerate the performance of rice plants being grown in SRI environments above and below ground.

Keywords

Microbes Rice Trichoderma System of Rice Intensification Symbiosis 

References

  1. Abul-Baki AA, Anderson JD (1973) Vigour determination in soybean by multiple criteria. Crop Sci 3:630–637CrossRefGoogle Scholar
  2. Adak A, Prasanna R, Babu S, Bidyarani N, Verma S, Pal M, Shivay YS, Nain L (2016) Micronutrient enrichment mediated by plant-microbe interactions and rice cultivation practices. J Plant Nutr. doi:10.1080/01904167.2016.1148723 Google Scholar
  3. Anas I, Rupela OP, Thiyagarajan TM, Uphoff N (2011) A review of studies on SRI effects on beneficial organisms in rice soil rhizospheres. Paddy Water Environ 9:53–64CrossRefGoogle Scholar
  4. Benítez T, Rincón AM, Limón MC, Codón AC (2004) Biocontrol mechanisms of Trichoderma strains. Int Microbiol 7(4):249–260PubMedGoogle Scholar
  5. Björkman T (2004) Effect of Trichoderma colonization on auxin-mediated regulation of root elongation. Plant Growth Regul 43(1):89–92CrossRefGoogle Scholar
  6. Björkman T, Blanchard LM, Harman GE (1998) Growth enhancement of shrunken-2 (sh2) sweet corn by Trichoderma harzianum 1295–22: Effect of environmental stress. J Am Soc Hortic Sci 123(1):35–40Google Scholar
  7. Cai F, Yu G, Wang P, Wei Z, Fu L, Shen Q, Chen W (2013) Harzianolide, a novel plant growth regulator and systemic resistance elicitor from Trichoderma harzianum. Plant Physiol Biochem 73:106–113CrossRefPubMedGoogle Scholar
  8. Ceesay M, Reid WS, Fernandes ECM, Uphoff N (2006) The effects of repeated soil wetting and drying on lowland rice yield with System of Rice Intensification (SRI) methods. Int J Agric Sustain 4:5–14Google Scholar
  9. Chowdappa P, Kumar SM, Lakshmi MJ, Upreti KK (2013) Growth stimulation and induction of systemic resistance in tomato against early and late blight by Bacillus subtilis OTPB1 or Trichoderma harzianum OTPB3. Biol Control 65(1):109–117CrossRefGoogle Scholar
  10. 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(3):1579–1592CrossRefPubMedPubMedCentralGoogle Scholar
  11. 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):503–514Google Scholar
  12. 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(2):425–432CrossRefGoogle Scholar
  13. De Santiago A, Quintero JM, Avilés M, Delgado A (2011) Effect of Trichoderma asperellum strain T34 and glucose addition on iron, copper, manganese, and zinc uptake by wheat grown on calcareous medium. Plant Soil 342:97–104CrossRefGoogle Scholar
  14. de Souza R, Meyer J, Schoenfeld R, da Costa PB, Passaglia LM (2015) Characterization of plant growth-promoting bacteria associated with rice cropped in iron-stressed soils. Ann Microbiol 65(2):951–964CrossRefGoogle Scholar
  15. 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 4:45 doi:10.1186/s13568-014-0045-8
  16. Druzhinina IS, Seidl-Seiboth V, Herrera-Estrella A, Horwitz BA, Kenerley CM, Monte E, Mukherjee PK, Zeilinger S, Grigoriev IV, Kubicek CP (2011) Trichoderma: The genomics of opportunistic success. Nat Rev Microbiol 9(10):749–759CrossRefPubMedGoogle Scholar
  17. Edwards J, Johnson C, Santos-Medellín C, Lurie E, Podishetty NK, Bhatnagar S, Eisen JA, Sundaresan V (2015) Structure, Variation, and assembly of the root-associated microbiomes of rice. P Natl Acad Sci USA 112(8): E911-E920Google Scholar
  18. Garcıa-Gil JC, Plaza C, Soler-Rovira P, Polo A (2000) Long-term effects of municipal solid waste compost application on soil enzyme activities and microbial biomass. Soil Biol Biochem 32(13):1907–1913CrossRefGoogle Scholar
  19. Gopalakrishnan S, Kumar RM, Humayun P, Srinivas V, Kumari BR, Vijayabharathi R, Singh A, Surekha K, Padmavathi C, Somashekar N, Rao PR (2014) Assessment of different methods of rice (Oryza sativa. L) Cultivation affecting growth parameters, soil chemical, biological, and microbiological properties, water saving, and grain yield in rice–rice system. Paddy Water Environ 12(1):79–87Google Scholar
  20. Gravel V, Antoun H, Tweddell RJ (2007) Growth stimulation and fruit yield improvement of greenhouse tomato plants by inoculation with Pseudomonas putida or Trichoderma atroviride: possible role of indole acetic acid (IAA). Soil Biol Biochem 39(8):1968–1977CrossRefGoogle Scholar
  21. Harman GE (2011) Multifunctional fungal plant symbionts: new tools to enhance plant growth and productivity. New Phytol 189:647–649CrossRefPubMedGoogle Scholar
  22. Harman GE, Howell CE, Viterbo A, Chet I, Lorito M (2004) Trichoderma species: Opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2(1):43–56CrossRefPubMedGoogle Scholar
  23. Hoyos-Carvajal L, Orduz S, Bissett J (2009) Growth stimulation in bean (Phaseolus vulgaris L.) by Trichoderma. Biol Control 51(3):409–416CrossRefGoogle Scholar
  24. IRRI (2011) Measuring Seed Germination. Postharvest Fact Sheets. http://www.knowledgebank.irri.org/factsheetsPDFs/CropEstablishment_Measuring%20Seed%20Germination.pdf (Accessed on 12 May 2014)
  25. Jiang X, Geng A, He N, Li Q (2011) New isolate of Trichoderma viride strain for enhanced cellulolytic enzyme complex production. J Biosci Bioeng 111(2):121–127CrossRefPubMedGoogle Scholar
  26. Kapri A, Tewari L (2010) Phosphate solubilization potential and phosphatase activity of rhizospheric. Trichoderma spp Braz J Microbiol 41(3):787–795Google Scholar
  27. Kaushish S, Kumar A, Aggarwal A, Parkash V (2012) Influence of inoculation with the endomycorrhizal fungi and Trichoderma viride on morphological and physiological growth parameters of Rauwolfia serpentina Benth. Ex Kurtz Indian J Microbiol 52(2):295–299CrossRefPubMedGoogle Scholar
  28. Li X, Bu N, Li Y, Ma L, Xin S, Zhang L (2012) Growth, photosynthesis and antioxidant responses of endophyte infected and non-infected rice under lead stress conditions. J Hazard Mater 213:55–61CrossRefPubMedGoogle Scholar
  29. Lifshitz R, Kloepper JW, Kozlowski M, Simonson C, Carlson J, Tipping EM, Zaleska I (1987) Growth promotion of canola (rapeseed) seedlings by a strain of Pseudomonas putida under gnotobiotic conditions. Can J Microbiol 5:390–395CrossRefGoogle Scholar
  30. López-Bucio J, Pelagio-Flores R, Herrera-Estrella A (2015) Trichoderma as biostimulant: exploiting the multilevel properties of a plant beneficial fungus. Sci Hortic 196:109–123Google Scholar
  31. Martínez-Medina A, Roldán A, Pascual JA (2011) Interaction between arbuscular mycorrhizal fungi and Trichoderma harzianum under conventional and low input fertilization field condition in melon crops: growth response and Fusarium wilt biocontrol. Appl Soil Ecol 47(2):98–105CrossRefGoogle Scholar
  32. Mishra A, Salokhe VM (2008) Seedling characteristics and the early growth of transplanted rice under different water regimes. Exp Agric 44(3):365–383CrossRefGoogle Scholar
  33. Mishra A, Salokhe VM (2011) Rice growth and physiological responses to SRI water management and implications for crop productivity. Paddy Water Environ 9:41–52CrossRefGoogle Scholar
  34. Muthukumarasamy R, Revathi G, Lakshminarasimhan C (1999) Influence of N fertilisation on the isolation of Acetobacter diazotrophicus and Herbaspirillum spp. from Indian sugarcane varieties. Biol Fertil Soils 29(2):157–164CrossRefGoogle Scholar
  35. Neumann B, Laing M (2006) Trichoderma: An ally in the quest for soil system sustainability. In: Biological Approaches to Sustainable Soil Systems, Uphoff N, Fernandes E, Herren H, Husson O, Laing M, Palm C, Pretty J, Sanchez P, Sanginga N, Thies J (Eds.). Boca Raton, FL: CRC Press. 491–500Google Scholar
  36. Pallai R, Hynes RK, Verma B, Nelson LM (2012) Phytohormone production and colonization of canola (Brassica napus L.) roots by Pseudomonas fluorescens 6–8 under gnotobiotic conditions. Can J Microbiol 58(2):170–178Google Scholar
  37. Pariona-Llanos R, de Santi Ferrara FI, Gonzales HHS, Barbosa HR (2010) Influence of organic fertilization on the number of culturable diazotrophic endophytic bacteria isolated from sugarcane. Eur J Soil Biol 46(6):387–393CrossRefGoogle Scholar
  38. Pérez-Harguindeguy N, Díaz S, Garnier E, Lavorel S, Poorter H, Jaureguiberry P, Bret-Harte MS, Cornwell WK, Craine JM, Gurvich DE, Urcelay C (2013) New handbook for standardised measurement of plant functional traits worldwide. Aus J Bot 61(3):167–234CrossRefGoogle Scholar
  39. Plaza C, Hernández D, Garcia-Gil JC, Polo A (2004) Microbial activity in pig slurry-amended soils under semiarid conditions. Soil Biol Biochem 36(10):1577–1585CrossRefGoogle Scholar
  40. Porras M, Barrau C, Romero F (2007) Effects of soil solarization and Trichoderma on strawberry production. Crop Prot 26(5):782–787CrossRefGoogle Scholar
  41. Prasanna R, Adak A, Verma S, Bidyarani N, Babu S, Pal M, Shivay YS, Nain L (2015) Microbial inoculation in rice grown under flooded and SRI modes of cultivation elicits differential effects on plant growth and nutrient dynamics. Ecol Eng 84:532–541CrossRefGoogle Scholar
  42. 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):e14823Google Scholar
  43. 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):404–416CrossRefPubMedGoogle Scholar
  44. Rodriguez RJ, Freeman DC, McArthur ED, Kin YO, Redman RS (2009) Symbiotic regulation of plant growth, development and reproduction. Communicative & Integr Biol 2(3): 1–3.Google Scholar
  45. 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(21):3943–3952CrossRefPubMedGoogle Scholar
  46. Shibghatallah MAH, Khotimah SN, Suhandono S, Viridi S, Kesuma T (2013) Measuring leaf chlorophyll concentration from its color: a way in monitoring environment change to plantations. AIP Conf Proc 1554(210). doi:10.1063/1.4820322
  47. Shoresh M, Harman GE, Mastouri F (2010) Induced systemic resistance and plant responses to fungal biocontrol agents. Annu Rev Phytopathol 48:21–43CrossRefPubMedGoogle Scholar
  48. 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 54:78–88CrossRefPubMedGoogle Scholar
  49. Simons M, Van Der Bij AJ, Brand I, De Weger LA, Wijffelman CA, Lugtenberg BJ (1996) Gnotobiotic system for studying rhizosphere colonization by plant growth-promoting Pseudomonas bacteria. Mol Plant-Microbe Interact 7:600–607Google Scholar
  50. Stevenson DM, Weimer PJ (2002) Isolation and characterization of a Trichoderma strain capable of fermenting cellulose to ethanol. Appl Microbiol Biotechnol 59:721–726CrossRefPubMedGoogle Scholar
  51. Thakur AK, Uphoff N, Antony E (2010a) An assessment of physiological effects of System of Rice Intensification (SRI) practices compared with recommended rice cultivation practices in India. Exp Agric 46(1):77–98CrossRefGoogle Scholar
  52. Thakur AK, Rath S, Roychowdhury S, Uphoff N (2010b) Comparative performance of rice with system of rice intensification (SRI) and conventional management using different plant spacings. J Agron Crop Sci 196(2):146–159CrossRefGoogle Scholar
  53. Thakur AK, Uphoff NT, Stoop WA (2016) Scientific underpinnings of the System of Rice Intensification (SRI): What is known so far? Adv Agron 135:147–179CrossRefGoogle Scholar
  54. Unger IM, Kennedy AC, Muzika RM (2009) Flooding effects on soil microbial communities. Appl Soil Ecol 42(1):1–8CrossRefGoogle Scholar
  55. Uphoff N, Chi F, Dazzo FB, Rodriguez RJ (2013) Soil fertility as a contingent rather than inherent characteristic: Considering the contributions of crop-symbiotic soil biota. In: Lal R, Stewart BA (eds) Boca Raton. CRC Press, FL, pp. 141–166Google Scholar
  56. Vinale F, Flematti G, Sivasithamparam K, Lorito M, Marra R, Skelton BW, Ghisalberti EL (2009) Harzianic acid, an antifungal and plant growth promoting metabolite from Trichoderma harzianum. J Nat Prod 72(11):2032–2035CrossRefPubMedGoogle Scholar
  57. Wani ZA, Ashraf N, Mohiuddin T, Riyaz-Ul-Hassan S (2015) Plant-endophyte symbiosis, an ecological perspective. Appl Microbiol Biotechnol 99(7):2955–2965CrossRefPubMedGoogle Scholar
  58. Watanarojanaporn N, Boonkerd N, Tittabutr P, Longtonglang A, Young JPW, Teaumroong N (2013) Effect of rice cultivation systems on indigenous arbuscular mycorrhizal fungal community structure. Microbes Environ 28:316–324CrossRefPubMedPubMedCentralGoogle Scholar
  59. Wu W, Uphoff N (2015) A review of the system of rice intensification in China. Plant Soil 393:361–381Google Scholar
  60. Yanni YG, Rizk RY, El-Fattah FK, Squartini A, Corich V, Giacomini A, de Bruijn F, Rademaker J, Maya-Flores J, Ostrom P, Vega-Hernandez M (2001) The beneficial plant growth-promoting association of Rhizobium leguminosarum bv. trifolii with rice roots. Austral J Plant Physiol 28:845–870Google Scholar
  61. 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(2):235–242CrossRefGoogle Scholar
  62. Yoshida S, Forno DA, Cock JH, Gomez KA (1976) Laboratory Manual for Physiological Studies of Rice. International Rice Research Institute (IRRI), Manila, PhilippinesGoogle Scholar
  63. Yuan ZL, Dai CC, Xia L, Tian LS, Wang XX (2007) Extensive host range of an endophytic fungus affects the growth and physiological functions in rice (Oryza sativa L.). Symbiosis 43(1):21–28Google Scholar
  64. Zhao L, Wu L, Li Y, Animesh S, Zhu D, Uphoff N (2010) Comparisons of yield, water use efficiency, and soil microbial biomass as affected by the System of Rice Intensification. Commun Soil Sci Plant Anal 41(1):1–12CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  1. 1.School of Biosciences and Biotechnology, Faculty of Science and TechnologyUniversiti Kebangsaan MalaysiaBangiMalaysia
  2. 2.School of Enviromental Sciences and Natural Resources, Faculty of Science and TechnologyUniversiti Kebangsaan MalaysiaBangiMalaysia
  3. 3.Department of Agrotechnology, Faculty of AgricultureUniversitas Islam RiauPekanbaruIndonesia
  4. 4.SRI International Network and Resources CenterCornell UniversityIthacaUSA

Personalised recommendations