Please wait a minute...
Journal of Integrative Agriculture  2021, Vol. 20 Issue (5): 1266-1276    DOI: 10.1016/S2095-3119(20)63415-3
Special Issue: Horticulture — Genetics · Breeding
Horticulture Advanced Online Publication | Current Issue | Archive | Adv Search |
Transcriptomic insights into growth promotion effect of Trichoderma afroharzianum TM2-4 microbial agent on tomato plants
ZHAO Juan, LIU Ting, LIU Wei-cheng, ZHANG Dian-peng, DONG Dan, WU Hui-ling, ZHANG Tao-tao, LIU De-wen
Institute of Plant and Environment Protection, Beijing Academy of Agriculture and Forestry Sciences, Beijing 100097, P.R.China
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
Plant growth promoting fungi are receiving increased attention as valuable beneficial microorganisms in crop cultivation due to their capacity to produce bioactive substances, promote plant growth and enhance immune defense functions.  In this study, a novel Trichoderma isolate, designated as TM2-4, was screened from healthy tomato rhizosphere soil and identified as Trichoderma afroharzianum.  Culture filtrate of the isolate TM2-4 displayed obvious bioactive substance production and an evident effect in promoting tomato seed germination, with hypocotyl length, radical length and vigor index increased by 28.7, 19.4 and 62.1%, respectively, after a 100-fold dilution treatment.  To assess the promotion effect and related mechanism of isolate TM2-4, the plant biological indexes and gene expression profiles of tomato plants treated with or without T. afroharzianum TM2-4 microbial agent were investigated by greenhouse pot experiment and RNA sequencing.  The results demonstrated that T. afroharzianum TM2-4 significantly promoted tomato plant growth in terms of plant height, dry weight, number of leaves per plant and root activity, through efficient colonization in the rhizosphere and root system of the plants.  Transcriptome analyses identified a total of 984 differentially expressed genes in T. afroharzianum microbial agent inoculated tomato roots, which were mainly engaged in the biological process of phytohormone homeostasis, antioxidant activity, as well as metabolic pathways including phenylpropanoid biosynthesis and glutathione metabolism.  These findings provide useful information for understanding the mechanism of isolate TM2-4 for tomato plant growth promotion, which would facilitate further development of T. afroharzianum TM2-4 microbial agent for use in vegetable crop production.
Keywords:  Trichoderma afroharzianum        Solanum lycopersicum L.        plant growth promotion        transcriptome analyses        qRT-PCR  
Received: 03 January 2020   Accepted: 12 April 2021
Fund: This research was supported by the Youth Research Fund of Beijing Academy of Agriculture and Forestry Sciences, China (QNJJ201814), the National Key R&D Program of China (2017YFD0201102), and the Beijing Key Laboratory of Green Control of Fruit Tree Diseases and Pests in the North China (BZ0432).
Corresponding Authors:  Correspondence LIU Ting, Tel/Fax: +86-10-51503337, E-mail:    
About author:  ZHAO Juan, E-mail:;

Cite this article: 

ZHAO Juan, LIU Ting, LIU Wei-cheng, ZHANG Dian-peng, DONG Dan, WU Hui-ling, ZHANG Tao-tao, LIU De-wen. 2021. Transcriptomic insights into growth promotion effect of Trichoderma afroharzianum TM2-4 microbial agent on tomato plants. Journal of Integrative Agriculture, 20(5): 1266-1276.

Achal V, Savant V V, Reddy M S. 2007. Phosphate solubilization by a wild type strain and UV-induced mutants of Aspergillus tubingensis. Soil Biology and Biochemistry, 39, 695–699.
Adiyadolgor T, Dávid R, Aruna V, Sándor K, Huynh T, Ágnes S, László B, Biljana D, Enkh-Amgalan J, Csaba V, András S. 2020. Characterization of the plant growth-promoting activities of endophytic fungi isolated from Sophora flavescens. Microorganisms, 8, 683.
Ashmita T, Touseef F, Anshu G, Udit Y, Suchi S, Poonam C S. 2018. Effect of Trichoderma koningiopsis on chickpea rhizosphere activities under different fertilization regimes. Open Journal of Soil Science, 8, 261–275.
Ben A M, Lopez D, Triki M A, Khouaja A, Chaar H, Fumanal B, Gousset-Dupont A, Bonhomme L, Label P, Goupil P, Ribeiro S, Pujade-Renaud V, Julien J L, Auguin D, Venisse J S. 2017. Beneficial effect of Trichoderma harzianum strain Ths97 in biocontrolling Fusarium solani causal agent of root rot disease in olive trees. Biological Control, 110, 70–78.
Cai F, Chen W, Wei Z. 2015. Colonization of Trichoderma harzianum strain SQR-T037 on tomato roots and its relationship to plant growth, nutrient availability and soil microflora. Plant and Soil, 388, 337–350.
Camilios-Neto D, Paloma B, Roseli W, Michelle Z T, Liziane C B, Glaucio V, Lucélia D, Helisson F, Vinicius A W, Leda S C, Fábio O P, Emanuel M S. 2014. Dual RNA-seq transcriptional analysis of wheat roots colonized by Azospirillum brasilense reveals up-regulation of nutrient acquisition and cell cycle genes. BMC Genomics, 15, 378.
Contreras-Cornejo H A, Macías-Rodríguez L, Del-Val E L J. 2018. The root endophytic fungus Trichoderma atroviride induces foliar herbivory resistance in maize plants. Applied Soil Ecology, 124, 45–53.
Coppola M, Diretto G, Digilio M C, Woo S L, Giuliano G, Molisso D, Pennacchio F, Lorito M, Rao R. 2019. Transcriptome and metabolome reprogramming in tomato plants by Trichoderma harzianum strain T22 primes and enhances defence responses against aphids. Frontiers in Physiology, 10, 745.
Doni F, Fathurrahman F, Mispan M S, Suhaimi N S M, Yusoff W M W, Uphoff N. 2019. Transcriptomic profiling of rice seedlings inoculated with the symbiotic fungus Trichoderma asperellum SL2. Journal of Plant Growth Regulation, 38, 1507–1515.
Elad Y, Chet I. 1983. Improved selective media for isolation of Trichoderma spp. or Fusarium spp. Phytoparasitica, 11, 55–58.
Gamez R M, Rodríguez F, Vidal N M, Ramirez S, Alvarez R V, Landsman D, Mariño-Ramírez L. 2019. Banana (Musa acuminata) transcriptome profiling in response to rhizobacteria: Bacillus amyloliquefaciens Bs006 and Pseudomonas fluorescens Ps006. BMC Genomics, 20, 378.
Gams W, Bisset J. 2002. Morphology and identification of Trichoderma. In: Kubicek C P, Herman C E, eds., Trichoderma and Gliocladium: Basic Biology Taxonomy and Genetics. Taylor and Francis, London. pp. 3–31.
Gordon S A, Weber R P. 1951. Colorimetric estimation of indole acetic acid. Plant Physiology, 26, 192–195.
Hernández-Herrera R M, Santacruz-Ruvalcaba F, Ruiz-López M A, Norrie J, Hernández-Carmona G. 2014. Effect of liquid seaweed extracts on growth of tomato seedlings (Solanum lycopersicum L.). Journal of Applied Phycology, 26, 619–628.
ISTA (International Seed Testing Association). 2005. International Rules for Seed Testing. The International Seed Testing Association, Switzerland.
Li Z, Janisiewicz W, Liu Z, Callahan A, Evans B, Jurick W, Dardick C. 2018. Exposure in vitro to an environmentally isolated strain TC09 of Cladosporium sphaerospermum triggers plant growth promotion, early flowering and fruit yield increase. Frontiers in Plant Science, 9, 1959.
Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method. Methods, 25, 402–408.
Machuca A, Milagres A M F. 2003. Use of CAS-agar plate modified to study the effect of different variables on the siderophore production by Aspergillus. Letters in Applied Microbiology, 36, 177–181.
Malinovsky F G, Fangel J U, Willats W G. 2014. The role of the cell wall in plant immunity. Frontiers in Plant Science, 5, 178.
Mao X Z, Cai T, Olyarchuk J G, Wei L P. 2005. Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics, 21, 3787–3793.
Maurya D P, Singh D, Pratap D, Maurya J P. 2012. Optimization of solid state fermentation conditions for the production of cellulase by Trichoderma reesei. Journal of Environmental Biology, 33, 5–8.
Mengistie B T, Mol A P J, Oosterveer P. 2017. Pesticide use practices among smallholder vegetable farmers in Ethiopian Central Rift Valley. Environment Development and Sustainability, 19, 301–324.
Moya P, Barrera V, Cipollone J, Bedoya C, Kohan L, Toledo A, Sisterna M N. 2020. New isolates of Trichoderma spp. as biocontrol and plant growth-promoting agents in the pathosystem Pyrenophora teres–barley in Argentina. Biological Control, 141, 104152.
Nautiyal C S. 1999. An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiology Letters, 170, 265–270.
Nawrocka J, Malolepsza U. 2013. Diversity in plant systemic resistance induced by Trichoderma. Biological Control, 67, 149–156.
Otieno N, Lally R D, Kiwanuka S, Lloyd A, Ryan D, Germaine K J, Dowling D N. 2015. Plant growth promotion induced by phosphate solubilizing endophytic Pseudomonas isolates. Frontiers in Microbiology, 6, 745.
De Palma M, Salzano M, Villano C, Aversano R, Lorito M, Ruocco M, Docimo T, Piccinelli A L, Agostino N, Tucci M. 2019. Transcriptome reprogramming, epigenetic modifications and alternative splicing orchestrate the tomato root response to the beneficial fungus Trichoderma harzianum. Horticulture Research, 6, 5.
Pascale A, Vinale F, Manganiello G, Nigro M, Lanzuise S, Ruocco M, Marra R, Lombardi N, Woo S L, Lorito M. 2017. Trichoderma and its secondary metabolites improve yield and quality of grapes. Crop Protection, 92, 176–181.
Perveen R, Suleria H A R, Anjum F M, Butt M S, Pasha I, Ahmad S. 2015. Tomato (Solanum lycopersicum) carotenoids and lycopenes chemistry; metabolism, absorption, nutrition, and allied health claims - A comprehensive review. Critical Reviews in Food Science and Nutrition, 55, 919–929.
Rodriguez R J, Henson J, Van Volkenburgh E, Hoy M, Wright L, Beckwith F, Kim Y O, Redman R S. 2008. Stress tolerance in plants via habitat-adapted symbiosis. The ISME Journal, 2, 404–416.
Saad S E, Tohamy A T, Khalid A H. 2020. Role of plant-growth promoting fungi (PGPF) in defensive genes expression of Triticum aestivum against wilt disease. Rhizosphere, 15, 100223.
Samuels G J, Dodd S L, Gams W. 2002. Trichoderma species associated with the green mold epidemic of commercially grown Agaricus bisporus. Mycologia, 94, 146–170.
Sawant I S, Wadkar P N, Ghule S B, Rajguru Y R, Salunkhe V P, Sawant S D. 2017. Enhanced biological control of powdery mildew in vineyards by integrating a strain of Trichoderma afroharzianum with sulphur. Biological Control, 114, 133-143.
Shukla N, Awasthi R P, Rawat L, Kumar J. 2012. Biochemical and physiological responses of rice (Oryza sativa L.) as influenced by Trichoderma harzianum under drought stress. Plant Physiology and Biochemistry, 54, 78–88.
Sugimura Y, Saito K. 2017. Comparative transcriptome analysis between Solanum lycopersicum L. and Lotus japonicus L. during arbuscular mycorrhizal development. Soil Science and Plant Nutrition, 63, 127–136.
Swofford D L. 2002. PAUP*: Phylogenetic analysis using parsimony (* and other methods). Version 4.0b10. Sinauer Associates, Sunderland.
Trapnell C, Williams B A, Pertea G, Mortazavi A, Kwan G, Van Baren M J, Salzberg S L, Wold B J, Pachter L. 2010. Transcript assembly and quantification by RNA-seq reveals unannotated transcripts and isoform switching during cell differentiation. Nature Biotechnology, 28, 511–515.
Underwood W. 2012. The plant cell wall: A dynamic barrier against pathogen invasion. Frontiers in Plant Science, 3, 1–6.
Varshney R K, Nayak S N, May G D, Jackson S A. 2009. Next-generation sequencing technologies and their implications for crop genetics and breeding. Trends in Biotechnology, 27, 522–530.
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 Microbiology Letters, 305, 42–48.
Wang N, Gao Y, Wang Y H, Li X F. 2016. Adoption of eco-friendly soil-management practices by smallholder farmers in Shandong Province of China. Soil Science and Plant Nutrition, 62, 185–193.
Wani Z A, Ashraf N, Mohiuddin T, Riyaz-UI-Hassan S. 2015. Plant-endophyte symbiosis, an ecological perspective. Applied Microbiology and Biotechnology, 99, 2955–2965.
White T J, Bruns T D, Lee S, Taylor J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes. In: Innis M A, Gelfand D H, Sninsky J J, White T J, eds., PCR Protocols: A Guide to Methods and Applications. Academic Press, San Diego. pp. 315–322.
Wu Y W, Li Q, Jin R, Chen W, Liu X L, Kong F L, Ke Y P, Shi H C, Yuan J C. 2019. Effect of low-nitrogen stress on photosynthesis and chlorophyll fluorescence characteristics of maize cultivars with different low-nitrogen tolerances. Journal of Integrative Agriculture, 18, 1246–1256.
Young M D, Wakefield M J, Smyth G K, Oshlack A. 2010. Gene ontology analysis for RNA-seq: Accounting for selection bias. Genome Biology, 11, R14.
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.
Zhao J, Liu W C, Liu D W, Lu C G, Zhang D P, Wu H L, Dong D, Meng L L. 2018. Identification and evaluation of Aspergillus tubingensis as a potential biocontrol agent against grey mould on tomato. Journal of General Plant Pathology, 84, 148–159.
Zhao J, Xue Q H, Shen G H, Xue L, Duan J L, Wang D S. 2012. Evaluation of Streptomyces spp. for biocontrol of gummy stem blight (Didymella bryoniae) and growth promotion of Cucumis melo L. Biocontrol Science and Technology, 22, 23–37.
[1] LUO Jing, MA Chao, LI Zhe, ZHU Bang-qin, ZHANG Jiang, LEI Chao-liang, JIN Shuang-xia, J. Joe Hull, CHEN Li-zhen. Assessment of suitable reference genes for qRT-PCR analysis in Adelphocoris suturalis[J]. >Journal of Integrative Agriculture, 2018, 17(12): 2745-2757.
[2] Sumaira Farrakh, Meinan Wang, Xianming Chen. Pathogenesis-related protein genes involved in race-specific allstage resistance and non-race specific high-temperature adult-plant resistance to Puccinia striiformis f. sp. tritici in wheat[J]. >Journal of Integrative Agriculture, 2018, 17(11): 2478-2491.
No Suggested Reading articles found!