Skip to main content

Roles of microbes in supporting sustainable rice production using the system of rice intensification

Applied Microbiology and Biotechnology volume 103, pages 5131–5142 (2019)Cite this article

Abstract

The system of rice intensification (SRI) is an agroecological approach to rice cultivation that seeks to create optimal conditions for healthy plant growth by minimizing inter-plant competition, transplanting widely spaced young single seedlings, and optimizing favorable soil conditions with organic amendments, increased soil aeration by weeding, and controlled water management. These practices improve rice plant growth with yields up to three times more than with conventional cultivation methods, and increase crop resilience under biotic and abiotic stresses. This review discusses the roles of beneficial microbes in improving rice plant growth, yield, and resilience when SRI practices are used, and how these modifications in plant, soil, water, and nutrient management affect the populations and diversity of soil microorganisms. Mechanisms whereby symbiotic microbes support rice plants’ growth and performance are also discussed.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3

References

  • 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 39:1216–1232

    Article  CAS  Google Scholar 

  • Al-Shorgani NKN, Isa MHM, Yusoff WMW, Kalil MS, Hamid AA (2016) Isolation of a Clostridium acetobutylicum strain and characterization of its fermentation performance on agricultural wastes. Renew Energy 86:459–465

    Article  CAS  Google Scholar 

  • Al-Taweil HIB, Osman M, Hamid AA, Wan Mohtar WY (2009) Development of microbial inoculants and the impact of soil application on rice seedlings growth. Am J Agri Biol Sci 4:79–82

    Article  Google Scholar 

  • 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 9:53–64

    Article  Google Scholar 

  • Badri DV, Weir TL, van der Lelie D, Vivanco JM (2009) Rhizosphere chemical dialogues: plant–microbe interactions. Curr Opin Biotechnol 20:642–650

    Article  CAS  PubMed  Google Scholar 

  • Baez-Rogelio A, Morales-García YE, Quintero-Hernández V, Muñoz-Rojas J (2017) Next generation of microbial inoculants for agriculture and bioremediation. Microb Biotechnol 10:19–21

    Article  PubMed  Google Scholar 

  • Barea JM, Azcon R, Azcon-Aguilar C (2002) Mycorrhizosphere interactions to improve plant fitness and soil quality. Antonie van Leeuwenhoek 81:343–351

    Article  CAS  PubMed  Google Scholar 

  • Barison J, Uphoff N (2011) Rice yield and its relation to root growth and nutrient-use efficiency under SRI and conventional cultivation: an evaluation in Madagascar. Paddy Water Environ 9:65–78

  • Benitez T, Rincon AM, Limon MC, Codon AC (2004) Biocontrol mechanisms of Trichoderma strains. Int Microbiol 7:249–260

    CAS  PubMed  Google Scholar 

  • Berendsen RL, Pieterse CMJ, Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486

    Article  CAS  PubMed  Google Scholar 

  • Bhardwaj D, Ansari MW, Sahoo RK, Tuteja N (2014) Biofertilizers function as key player in sustainable agriculture by improving soil fertility, plant tolerance and crop productivity. Microb Cell Fact 13:66

    Article  PubMed  PubMed Central  Google Scholar 

  • Bhattacharyya PN, Jha DK (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microbiol Biotechnol 28:1327–1350

    Article  CAS  PubMed  Google Scholar 

  • Blaser MJ, Cardon ZC, Cho MK, Dangl JL, Donohue TJ, Green JL, Knight R, Maxon ME, Northen TR, Pollard KS, Brodie EL (2016) Toward a predictive understanding of Earth's microbiomes to address 21st century challenges. mBio 7:e00714–00716

  • 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 51:1969–1977

    Article  CAS  PubMed  Google Scholar 

  • Busby PE, Soman C, Wagner MR, Friesen ML, Kremer J, Bennett A, Morsy M, Eisen JA, Leach JE, Dangl JL (2017) Research priorities for harnessing plant microbiomes in sustainable agriculture. PLoS Biol 15:e2001793

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cassan F, Bottini R, Schneider G, Piccoli P (2001) Azospirillum brasilense and Azospirillum lipoferum hydrolyze conjugates of GA20 and metabolize the resultant aglycones to GA1 in seedlings of rice dwarf mutants. Plant Physiol 125:2053–2058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cassman KG, Peng S, Olk DC, Ladha JK, Reichardt W, Dobermann A, Singh U (1998) Opportunities for increased nitrogen-use efficiency from improved resource management in irrigated rice systems. Field Crops Res 56:7–39

    Article  Google Scholar 

  • Chapagain T, Yamaji E (2010) The effects of irrigation method, age of seedling and spacing on crop performance productivity and water-wise rice production in Japan. Paddy Water Environ 8:81–90

    Article  Google Scholar 

  • Chebotar VK, Malfanova NV, Shcherbakov AV, Ahtemova GA, Borisov AY, Lugtenberg B, Tikhonovich IA (2015) Endophytic bacteria in microbial preparations that improve plant development (review). Appl Biochem Microbiol 51:271–277

    Article  CAS  Google Scholar 

  • Chen LH, Zhang J, Shao XH, Wang SS, Miao QS, Mao XY, Zhai YM, She DL (2015) Development and evaluation of Trichoderma asperellum preparation for control of sheath blight of rice (Oryza sativa L.). Biocontrol Sci Technol 25:316–328

    Article  Google Scholar 

  • Chi F, Shen SH, Cheng HP, Jing YX, Yanni YG, Dazzo FB (2005) Ascending migration of endophytic rhizobia, from roots to leaves, inside rice plants and assessment of benefits to rice growth physiology. Appl Environ Microbiol 71:7271–7278

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chi F, Yang P, Han F, Jing Y, Shen S (2010) Proteomic analysis of rice seedlings infected by Sinorhizobium meliloti 1021. Proteomics 10:1861–1874

    Article  CAS  PubMed  Google Scholar 

  • Choi J, Kim G, Park W, Shin M, Choi Y, Lee S, Kim S, Yun D (2014) Effect of SRI water management on water quality and greenhouse gas emissions in Korea. Irrig Drain 63:263–270

    Article  Google Scholar 

  • Compant S, Duffy B, Jerzy N, Clement C, Barka EA (2005) Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl Environ Microbiol 71:4951–4959

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doni F, Anizan I, Che Radziah CMZ, Wan Mohtar WY (2014a) Physiological and growth response of rice (Oryza sativa L.) plants to Trichoderma spp. inoculants. AMB Express 4:45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doni F, Anizan I, Che Radziah CMZ, Wan Natasha WM, Abidah A, Suryadi E, Wan Mohtar WY (2014b) Enhanced rice seedling growth by Clostridium and Pseudomonas. Biotechnol 13:186–189

    Article  CAS  Google Scholar 

  • 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 72:45–59

    Article  CAS  Google Scholar 

  • 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 8:207–223

    Article  Google Scholar 

  • Doni F, Fathurrahman F, Mispan MS, Suhaimi NSM, Yusoff WMW, Uphoff N (2019) Transcriptomic profiling of rice seedlings inoculated with the symbiotic fungus Trichoderma asperellum SL2. J Plant Growth Regul. https://doi.org/10.1007/s00344-019-09952-7

  • Drogue B, Sanguin H, Chamam A, Mozar M, Llauro C, Panaud O, Prigent-Combaret C, Picault N, Wisniewski-Dyé F (2014) Plant root transcriptome profiling reveals a strain-dependent response during Azospirillum-rice cooperation. Front Plant Sci 5:607

    Article  PubMed  PubMed Central  Google Scholar 

  • Duffy B, Keel C, Défago G (2004) Potential role of pathogen signaling in multitrophic plant-microbe interactions involved in disease protection. Appl Environ Microbiol 70:1836–1842

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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. Proc Natl Acad Sci USA 112:E911–E920

    Article  CAS  PubMed  Google Scholar 

  • Elshakh AS, Anjum SI, Qiu W, Almoneafy AA, Li W, Yang Z, Xie G (2016) Controlling and defence-related mechanisms of Bacillus strains against bacterial leaf blight of rice. J Phytopathol 164:534–546

    Article  CAS  Google Scholar 

  • Fagundes CT, Amaral FA, Teixeira AL, Souza DG, Teixeira MM (2012) Adapting to environmental stresses: the role of the microbiota in controlling innate immunity and behavioral responses. Immunol Rev 245:250–264

    Article  CAS  PubMed  Google Scholar 

  • FAO (2017) The State of Food and Agriculture. http://www.fao.org/3/a-i7658e.pdf Accessed 15 June 2018

  • Farré-Armengol G, Filella I, Llusia J, Peñuelas J (2016) Bidirectional interaction between phyllospheric microbiotas and plant volatile emissions. Trends Plant Sci 21:854–860

    Article  CAS  PubMed  Google Scholar 

  • Finkel OM, Castrillo G, Paredes SH, González IS, Dangl JL (2017) Understanding and exploiting plant beneficial microbes. Curr Opin Plant Biol 38:155–163

    Article  PubMed  PubMed Central  Google Scholar 

  • Gathorne-Hardy A, Reddy DN, Venkatanarayana M, Harriss-White B (2016) System of Rice Intensification provides environmental and economic gains but at the expense of social sustainability—a multidisciplinary analysis in India. Agr Syst 143:159–168

    Article  Google Scholar 

  • Gopalakrishnan S, Upadhyaya HD, Vadlamudi S, Humayun P, Vidya MS, Alekhya G, Singh A, Vijayabharathi R, Bhimineni RK, Seema M, Rathore A, Rupela O (2012) Plant growth-promoting traits of biocontrol potential bacteria isolated from rice rhizosphere. SpringerPlus 1:71

  • Gopalakrishnan S, Kumar R, Humayun P, Srinivas V, Kumari B, Vijayabharathi R, Singh A, Surekha K, Padmavathi C, Somashekar N, Rao P, Latha P, Rao L, Babu V, Viraktamath B, Goud V, Loganandhan N, Gujja B, Rupela O (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 12:79–87

    Article  Google Scholar 

  • Goswami D, Thakker JN, Dhandhukia PC, Tejada Moral M (2016) Portraying mechanics of plant growth promoting rhizobacteria (PGPR): a review. Cogent Food Agric 2:1127500

    Google Scholar 

  • Grayston SJ, Vaughan D, Jones D (1996) Rhizosphere carbon flow in trees, in comparison with annual plants: the importance of root exudation and its impact on microbial activity and nutrient availability. Appl Soil Ecol 5:29–56

    Article  Google Scholar 

  • Guimil S, Chang HS, Zhu T, Sesma A, Osbourn A, Roux C, Ioannidis V, Oakeley EJ, Docquier M, Descombes P, Briggs SP (2005) Comparative transcriptomics of rice reveals an ancient pattern of response to microbial colonization. Proc Natl Acad Sci USA 102:8066–8070

    Article  CAS  PubMed  Google Scholar 

  • Gutjahr C, Sawers RJ, Marti G, Andrés-Hernández L, Yang SY, Casieri L, Angliker H, Oakeley EJ, Wolfender JL, Abreu-Goodger C, Paszkowski U (2015) Transcriptome diversity among rice root types during asymbiosis and interaction with arbuscular mycorrhizal fungi. Proc Natl Acad Sci USA 112:6754–6759

    Article  CAS  PubMed  Google Scholar 

  • Hannah L, Steele M, Imbach P, Flint L, Flint A (2017) Climate change influences on pollinator, forest, and farm interactions across a climate gradient. Clim Chang 141:29–45

    Article  Google Scholar 

  • Harman GE (2011) Multifunctional fungal plant symbionts: new tools to enhance plant growth and productivity. New Phytol 189:647–649

    Article  PubMed  Google Scholar 

  • Harman G, Uphoff N (2019) Symbiotic root-endophytic soil microbes improve crop productivity and provide environmental benefits. Scientifica 9106395:1–25

    Article  Google Scholar 

  • Harman GE, Björkman T, Ondik K, Shoresh M (2008) Changing paradigms on the mode of action and uses of Trichoderma spp. for biocontrol. Outlook Pest Manag 19:24–29

    Article  Google Scholar 

  • Harman GE, Herrera-Estrella AH, Horwitz BA, Lorito M (2012) Special issue: Trichoderma – from basic biology to biotechnology. Microbiology 158:1–2

    Article  CAS  PubMed  Google Scholar 

  • Hastuti RD, Lestari Y, Suwanto A, Saraswati R (2012) Endophytic Streptomyces spp. as biocontrol agents of rice bacterial leaf blight pathogen (Xanthomonas oryzae pv. oryzae). Hayati J Biosci 19:155–162

    Article  Google Scholar 

  • Hu L, Robert CA, Cadot S, Zhang X, Ye M, Li B, Manzo D, Chervet N, Steinger T, Van Der Heijden MG, Schlaeppi K (2018) Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota. Nat Commun 9:2E738

  • Jagannath P, Pullabhotla H, Uphoff N (2013) Meta–analysis evaluating water use, water saving and water productivity in irrigated production of rice with SRI vs. standard management methods. Taiwan Water Conserv 61:14–49

    Google Scholar 

  • Jambon I, Thijs S, Weyens N, Vangronsveld J (2018) Harnessing plant-bacteria-fungi interactions to improve plant growth and degradation of organic pollutants. J Plant Interact 13:119–130

    Article  CAS  Google Scholar 

  • Kang S, Hao X, Du T, Tong L, Su X, Lu H, Li X, Huo Z, Li S, Ding RS (2017) Improving agricultural water productivity to ensure food security in China under changing environment: from research to practice. Agric Water Manag 2017:5–17

    Article  Google Scholar 

  • Khadka RB, Acharya P, Uphoff N (2014) Performance of landraces and improved varieties under the System of Rice Intensification management in Bajhang district of Nepal. J Agric Environ 15:1–10

  • Khadka RB, Uphoff N (2019) Effects of Trichoderma seedling treatment with System of Rice Intensification management and with conventional management of transplanted rice. Peer J 7:e5877

    Article  PubMed  Google Scholar 

  • Knief C, Delmotte N, Chaffron S, Stark M, Innerebner G, Wassmann R, von Mering C, Vorholt JA (2012) Metaproteogenomic analysis of microbial communities in the phyllosphere and rhizosphere of rice. ISME J 6:1378–1390

    Article  CAS  PubMed  Google Scholar 

  • Lareen A, Burton F, Schäfer P (2016) Plant root-microbe communication in shaping root microbiomes. Plant Mol Biol 90:575–587

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lauren JG, Duxbury JM (2005) Management strategies to reduce arsenic uptake by rice. In: Behavior of arsenic in aquifers, soils and plants. Conference Proceedings. International Symposium, Dhaka

    Google Scholar 

  • 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 213:55–61

    Article  CAS  PubMed  Google Scholar 

  • Lin X, Zhu D, Lin X (2011) Effects of water management and organic fertilization with SRI crop practices on hybrid rice performance and rhizosphere dynamics. Paddy Water Environ 9:33–39

    Article  Google Scholar 

  • Liu K, Garrett C, Fadamiro H, Kloepper JW (2016) Induction of systemic resistance in Chinese cabbage against black rot by plant growth-promoting rhizobacteria. Biol Control 99:8–13

    Article  Google Scholar 

  • Loeppmann S, Blagodatskaya E, Pausch J, Kuzyakov Y (2016) Substrate quality affects kinetics and catalytic efficiency of exo-enzymes in rhizosphere and detritusphere. Soil Biol Biochem 92:111–118

    Article  CAS  Google Scholar 

  • Lugtenberg BJJ, Caradus JR, Johnson LJ (2016) Fungal endophytes for sustainable crop production. FEMS Microbiol Ecol 92:fiw194

    Article  CAS  PubMed  Google Scholar 

  • Lugtenberg B, Rozen DE, Kamilova F (2017) Wars between microbes on roots and fruits. F1000Research 6:343

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mickan BS, Abbott LK, Solaiman ZM, Mathes F, Siddique KH, Jenkins SN (2019) Soil disturbance and water stress interact to influence arbuscular mycorrhizal fungi, rhizosphere bacteria and potential for N and C cycling in an agricultural soil. Biol Fertil Soils 55:53–66

    Article  CAS  Google Scholar 

  • Mishra A, Salokhe VM (2011) Rice growth and physiological responses to SRI water management and implications for crop productivity. Paddy Water Environ 9:41–52

    Article  Google Scholar 

  • 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 243:1251–1264

    Article  CAS  PubMed  Google Scholar 

  • Pangesti N, Reichelt M, van de Mortel JE, Kapsomenou E, Gershenzon J, van Loon JJA, Dicke M, Pineda A (2016) Jasmonic acid and ethylene signaling pathways regulate glucosinolate levels in plants during rhizobacteria-induced systemic resistance against a leaf-chewing herbivore. J Chem Ecol 42:1212–1225

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pedraza RO, Bellone CH, de Bellone SC, Sorte PMFB, dos Santos Teixeira KR (2009) Azospirillum inoculation and nitrogen fertilization effect on grain yield and on the diversity of endophytic bacteria in the phyllosphere of rice rainfed crop. European J Soil Biol 45:36–43

    Article  CAS  Google Scholar 

  • Peng S, Huang J, Zhong X, Yang J, Wang G, Zou Y, Zhang F, Zhu Q, Buresh R, Witt C (2002) Challenge and opportunity in improving fertilizer nitrogen use efficiency of irrigated rice in China. Agric Sci China 1:776–785

    Google Scholar 

  • 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 Engineering 84:532–541

    Article  Google Scholar 

  • Rahman SFSA, Singh E, Pieterse CMJ, Schenk PM (2018) Emerging microbial biocontrol strategies for plant pathogens. Plant Sci 267:102–111

    Article  CAS  Google Scholar 

  • Randriamiharisoa R, Barison J, Uphoff N (2006) Soil biological contributions to the System of Rice Intensification. 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. Florida, Boca Raton, pp 409–424

    Chapter  Google Scholar 

  • Ray DK, Ramankutty N, Mueller ND, West PC, Foley JA (2012) Recent patterns of crop yield growth and stagnation. Nat Commun 3:1293

    Article  CAS  PubMed  Google Scholar 

  • Reddy K, Reddy C, Muralidharan K (2009) Potential of botanicals and biocontrol agents on growth and aflatoxin production by Aspergillus flavus infecting rice grains. Food Control 20:173–178

    Article  CAS  Google Scholar 

  • Redman RS, Rodriguez RJ (2017) The symbiogenic tango: achieving climate-resilient crops via mutualistic plant-fungal relationships. In: Doty S (ed) Functional importance of the plant microbiome. Springer, Cham, pp 71–87

    Chapter  Google Scholar 

  • Redman RS, Dunigan DD, Rodriguez RJ (2001) Fungal symbiosis from mutualism to parasitism: who controls the outcome, host or invader? New Phytol 151:705–716

    Article  Google Scholar 

  • 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:e14823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reeves T, Thomas G, Ramsay G (2016) Save and grow in practice: maize, rice, wheat -- a guide to sustainable cereal production. UN Food and Agriculture Organization, Rome

  • Reinhold-Hurek B, Hurek T (1997) Azoarcus spp. and their interactions with grass roots. Plant Soil 194:57–64

    Article  CAS  Google Scholar 

  • Rodriguez RJ, Henson J, Van Volkenburgh E, Hoy M, Wright L, Beckwith F, Kim Y, Redman RS (2008) Stress tolerance in plants via habitat-adapted symbiosis. ISME J 2:404–416

    Article  PubMed  Google Scholar 

  • Rodriguez RJ, White JF Jr, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330

    Article  CAS  PubMed  Google Scholar 

  • Römheld V, Neumann G (2006) The rhizosphere: contributions of the soil-root interface to sustainable soil systems. 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. Florida, Boca Raton, pp 91–107

    Chapter  Google Scholar 

  • Sakthivel N, Gnanamanickam SS (1987) Evaluation of Pseudomonas fluorescens for suppression of sheath-rot disease and for enhancement of grain yields in rice (Oryza sativa L.). Appl Environ Microbiol 53:2056–2059

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sarker MA, Alam K, Gow J (2012) Exploring the relationship between climate change and rice yield in Bangladesh: an analysis of time series data. Agric Sys 112:11–16

    Article  Google Scholar 

  • Schlaeppi K, Bulgarelli D (2015) The plant microbiome at work. Mol Plant Microbe Interact 28:212–217

    Article  CAS  PubMed  Google Scholar 

  • Schulz B, Boyle C (2005) The endophytic continuum. Mycol Res 109:661–686

    Article  PubMed  Google Scholar 

  • Sessitsch A, Hardoim P, Doring J, Weilharter A, Krause A, Woyke T, Mitter B, Houberg-lotte L, Friedrich F, Rahalkar M, Hurek T, Sarkar A, Bodrossy L, van Overbeek L, Brar D, van Elsas JD, Reinhold-Hurek B (2012) Functional characteristics of an endophyte community colonizing rice roots as revealed by metagenomic analysis. Mol Plant Microbe Interact 25:28–36

    Article  CAS  PubMed  Google Scholar 

  • Shahane AA, Shivay YS, Prasanna R, Kumar D (2019) Improving water and nutrient use efficiency in rice by changing crop establishment methods, application of microbial inoculations, and Zn fertilization. Glob Chall 1800005:1–14

    Google Scholar 

  • 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 54:78–88

    Article  CAS  PubMed  Google Scholar 

  • Singh DP, Singh HB, Prabha R (2016) Microbial inoculants in sustainable agricultural productivity. Springer, New Delhi

    Book  Google Scholar 

  • Sooksa-Nguan T, Thies JE, Gypmantasiri P, Boonkerd N, Teaumroong N (2009) Effect of rice cultivation systems on nitrogen cycling and nitrifying bacterial community structure. Appl Soil Ecol 43:139–149

    Article  Google Scholar 

  • Sooksa-Nguan T, Gypmantasiri P, Boonkerd N, Thies JE, Teaumroong N (2010) Changes in bacterial community composition in the system of rice intensification (SRI) in Chiang Mai, Thailand. Microbes Environ 25:224–227

    Article  PubMed  Google Scholar 

  • Stoop WA, Uphoff N, Kassam A (2002) A review of agricultural research issue raised by the system of rice intensification (SRI) from Madagascar: opportunities for improving system for resource-poor farmers. Agric Syst 71:249–274

    Article  Google Scholar 

  • Stoop WA, Sabarmatee SP, Ravindra A, Sen D, Shambu Prasad C, Thakur AK (2017) Opportunities for ecological intensification: lessons and insights from the System of Rice/Crop Intensification – their implications for agricultural research and development approaches. CAB Reviews 12:1–19

    Article  Google Scholar 

  • Styger E, Uphoff N (2016) The system of rice intensification (SRI): revisiting agronomy for a changing climate. Climate-Smart Agriculture Practice Brief. CGIAR Research Program on Climate Change, Agriculture and Food Security, Copenhagen

    Google Scholar 

  • Suresh A, Ramesh M, Ram Reddy S (2014) Fluorescence pseudomonads contribute to the enhanced growth and yield under system of rice intensification (SRI). Indian J Agric Res 48:287–293

    Article  Google Scholar 

  • Thakur AK, Uphoff N, Antony E (2010) An assessment of physiological effects of System of Rice Intensification (SRI) practices compared with recommended rice cultivation practices in India. Exp Agric 46:77–98

    Article  Google Scholar 

  • Thakur AK, Uphoff N, Stoop WA (2016) Scientific underpinnings of the System of Rice Intensification (SRI): What is known so far? Adv Agron 135:147–179

    Article  Google Scholar 

  • Thakur AK, Mandal KG, Mohanty RK, Ambast SK (2018) Rice root growth, photosynthesis, yield and water productivity improvements through modifying cultivation practices and water management. Agric Water Manag 206:67–77

    Article  Google Scholar 

  • Timmusk S, Behers L, Muthoni J, Muraya A, Aronsson AC (2017) Perspectives and challenges of microbial application for crop improvement. Front Plant Sci 8:49

    Article  PubMed  PubMed Central  Google Scholar 

  • Turmel MS, Turner BL, Whalen JK (2011) Soil fertility and the yield response to the System of Rice Intensification. Renew Agr Food Syst 26:185–192

    Article  Google Scholar 

  • Turner T, James E, Poole P (2013) The plant microbiome. Genome Biol 14:209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • UN DESA (2015) World population prospects: the 2015 revision, key findings and advance tables Working Paper No ESA/P/WP.241

  • Uphoff N (2017) SRI: an agroecological strategy to meet multiple objectives with reduced reliance on inputs. Agroecol Sust Food 41:825–854

    Article  Google Scholar 

  • Uphoff N, Thakur AK (2019) In: Sarkar A, Sensasrma SR, VanLoon GW (eds) An agroecological strategy for adapting to climate change: the System of Rice Intensification (SRI). Sustainable Solutions for Food SecuritySpringer International Publishing, Basel, pp 229–254

    Google Scholar 

  • Vacher C, Hampe A, Porté AJ, Sauer U, Compant S, Morris CE (2016a) The phyllosphere: microbial jungle at the plant-climate interface. Annu Rev Ecol Evol Syst 47:1–24

    Article  Google Scholar 

  • Vacher C, Cordier T, Vallance J (2016b) Phyllosphere fungal communities differentiate more thoroughly than bacterial communities along an elevation gradient. Microb Ecol 72:1–3

    Article  PubMed  Google Scholar 

  • Venturi V, Keel C (2016) Signaling in the rhizosphere. Trends Plant Sci 21:187–198

    Article  CAS  PubMed  Google Scholar 

  • Vidhyasekaran P, Rabindran R, Muthamilan M, Nayar K, Rajappan K, Subramanian N, Vasumathi K (1997) Development of a powder formulation of Pseudomonas fluorescens for control of rice blast. Plant Pathol 46:291–297

    Article  Google Scholar 

  • Wani ZA, Ashraf N, Mohiuddin T, Riyaz-Ul-Hassan S (2015) Plant-endophyte symbiosis, an ecological perspective. Appl Microbiol Biotechnol 99:2955–2965

    Article  CAS  PubMed  Google Scholar 

  • 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 28:316–324

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 97:507–523

    Article  CAS  PubMed  Google Scholar 

  • Xuan VT (2018) Rice production, agricultural research, and the environment. In: Kerkvliet BJT, Porter DG (eds) Vietnam’s rural transformation. Routledge, Abingdon, pp 185–200

    Chapter  Google Scholar 

  • Yanni YG, Rizk RY, Corish V, Squartini A, Ninke K, Philip-Hollingsworth S, Orgambide G, de Bruijn F, Stoltzfus J, Buckley D, Schmidt TM, Mateos PF, Ladha JK, Dazzo FB (1997) Natural endophytic association between Rhizobium leguminosarum bv. trifolii and rice roots and assessment of its potential to promote rice growth. Plant Soil 194:99–114

  • Yasmin S, Hafeez FY, Mirza MS, Rasul M, Arshad HMI, Zubair M, Iqbal M (2017) Biocontrol of bacterial leaf blight of rice and profiling of secondary metabolites produced by rhizospheric Pseudomonas aeruginosa BRp3. Front Microbiol 8:1895

    Article  PubMed  PubMed Central  Google Scholar 

  • Yu YY, Jiang CH, Wang C, Chen LJ, Li HY, Xu Q, Guo JH (2017) An improved strategy for stable biocontrol agents selecting to control rice sheath blight caused by Rhizoctonia solani. Microbiol Res 203:1–9

    Article  PubMed  Google Scholar 

  • Yuan S, Nie L, Wang F, Huang J, Peng S (2017) Agronomic performance of inbred and hybrid rice cultivars under simplified and reduced-input practices. Field Crops Res 210:129–135

    Article  Google Scholar 

  • Zachow C, Berg C, Müller H, Monk J, Berg G (2016) Endemic plants harbour specific Trichoderma communities with an exceptional potential for biocontrol of phytopathogens. J Biotechnol 235:162–170

    Article  CAS  PubMed  Google Scholar 

  • Zhao LM, Wu LH, Li YS, Lu XH, Zhu DF, Uphoff N (2009) Influence of the system of rice intensification on rice yield and nitrogen and water use efficiency with different N application rates. Exp Agric 45:275–286

    Article  Google Scholar 

  • 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 Analy 41:1–12

    Article  CAS  Google Scholar 

  • Zhao C, Liu B, Piao S, Wang X, Lobell DB, Huang Y, Huang M, Yao Y, Bassu S, Ciais P, Durand JL, Elliott J, Ewert F, Janssens IA, Li T, Lin E, Liu Q, Martre P, Müller C, Peng S, Peñuelas J, Ruane AC, Wallach D, Wang T, Wu D, Liu Z, Zhu Y, Zhu Z, Asseng S (2017) Temperature increase reduces global yields of major crops in four independent estimates. Proc Natl Acad Sci USA 114:9326–9331

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This work was financially supported by the Ministry of Higher Education Malaysia under the Fundamental Research Grant Scheme FRGS/1/2015/SG03/UM/02/3, and University of Malaya under the Bantuan Kecil Penyelidikan BK004-2015 and the CEBAR fund RU006-2017.

Author information

Affiliations

  1. Institute of Biological Sciences, Faculty of Science, University of Malaya, 50603, Kuala Lumpur, Malaysia

    Febri Doni, Muhamad Shakirin Mispan, Nurul Shamsinah Mohd Suhaimi & Nazri Ishak

  2. Centre for Research in Biotechnology for Agriculture (CEBAR), University of Malaya, 50603, Kuala Lumpur, Malaysia

    Muhamad Shakirin Mispan

  3. SRI International Network and Resources Center, Cornell University, Ithaca, NY, 14853, USA

    Norman Uphoff

Authors
  1. Febri Doni
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Muhamad Shakirin Mispan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nurul Shamsinah Mohd Suhaimi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nazri Ishak
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Norman Uphoff
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Febri Doni or Muhamad Shakirin Mispan.

Ethics declarations

Ethical statement

This article does not contain any studies with human participants performed by any of the authors.

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Doni, F., Mispan, M.S., Suhaimi, N.S.M. et al. Roles of microbes in supporting sustainable rice production using the system of rice intensification. Appl Microbiol Biotechnol 103, 5131–5142 (2019). https://doi.org/10.1007/s00253-019-09879-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-019-09879-9

Keywords

  • Microbes
  • Plant–microbe interactions
  • Symbiosis
  • System of rice intensification