Abstract

The green revolution practiced at a great cost of environment to meet the ever-increasing demands for food and fiber. The indiscriminate use of agrochemicals resulted in a damaged ecosystem, food and water contamination, lost of local cultivar, pesticide tolerance, and disease resistance along with different climate change vulnerability. All these pressurize further on agricultural system to increase its productivity. Short-termed chemical remedy turns into today's hot topics of both environment and health concern. There is an urgent need to develop a sustainable approach for maximum crop production with minimum damage in climate vulnerable zone. Trichoderma are eco-friendly bio-reliance similar to organic and integrated management (IPM) recognized globally. In Bangladesh, the time is to avail Trichoderma as substitute of agrochemicals and fertilizers to combat biotic, abiotic both stresses. This study is for searching beneficial arsenal of Trichoderma to discover the whole tool box to counteract climate threat in rising demand of crop.

Keywords: Trichoderma; Fertilizers; Climate change; Agrochemicals.

Introduction

Trichoderma is a member of the largest group of fungi Ascomycota belonging to the Class Deuteromycetes. Trichoderma are soil born, free living, asexually reproducing filamentous fungi. Members of the genus are commonly isolated from soil and well known as avirulent plant symbiontas well as opportunistic invader. Kubicek et al. [1] explored its ubiquitousness and found Trichoderma as cosmopolitan and prevalent components of different ecosystem. They compete for food and site as a dominant component of soil microflora and predominantly occur in dead things and plant litter [2]. The high reproductive capacity with long self-lived profuse conidia, ability to grow under any irritable conditions, easy and inexpensive cultivation facilitates them to be used as a unique tool in organic agriculture. They also introduced as potential antagonist and being used as biopesticides globally for their driving force of disease suppressiveness to fungi and some nematodes. Apart from biocontrol aspect they nourished plant by solubilize plant nutrients, remediate pollutants and heavy metals thus impart abiotic stress tolerance. There are many products in market relying on microorganism but the inconsistency under field conditions and lack of proper information restricts their efficacy. It is necessary to know how Trichoderma interact with plant and other microbes to expand its use. Genome sequencing of Trichoderma species has done at certain level, provide data on understanding tetrahedron molecular interactions of mycoparasitism and Trichoderma-root symbiosis [3]. Now a wave of interest is addressed by growers and researchers to mitigate climate difficulty with a sustainable approach. We review the findings on several studies regarding environmental stress to un-mask and design a complete safeguard.

Rhizosphere Competence and Plant Root Colonization

The capabilities of microorganism to compete with others for nutrients secreted by roots and colonizing ability into root surface are termed rhizosphere competence. Plant rhizosphere is a complex ecological niche where a huge number of biological interactions occur and each organism struggles to survive here. Trichoderma are the key genus of Agricultural soil and rhizosphere is their common ecological niche as they are highly rhizosphere competent for availing both biotrophy and saprotrophy. Most soil inhibits the fungal germination and growth to a certain extent; the phenomenon is soil fungistasis. Trichoderma as dominant inhabitant are very successful to overcome fungistatic effect of soil and establish long-lasting colonization of plant root internally and externally. Organic compound exuded by root facilitates the plant to communicate with soil microorganism and Trichoderma secreted cysteinerich hydrophobin- like proteins [4] have been found to help them colonize and attach to plant roots. All beneficial traits of Trichoderma are intimately associated with the propound ability of species to grow and colonize in rhizosphere as well as free soil. Sometimes expansin like proteins with cellulose binding modules facilitates root penetration [5]. Once inside the root Trichoderma spp. must suppress plant defense mechanisms in order to create root invasion [6] and dubbed as a multifunctional endophytic plant symbiont.

Growth Promotion in Plants

Apart from the direct inhibition of plant pathogens, Trichoderma spp. is reported to improve crop health. Trichoderma draw nutrients from plants by facultative symbiosis, in return to boost fertility and immunity by coordinated transcriptomic, proteomic and metabolomic response in the plant [3]. Treatment with Trichoderma generally reduces the activity of deleterious microorganisms in the rhizosphere of plants, improves the nutrient status of soil and prevents the depletion of soil organic matter to sustain fertility. Secretion of hormone-like metabolites of plants stimulated by Trichoderma and release of nutrients from soil or organic matter has been proposed as the mechanisms involved in plant growth promotion. Secondary metabolites produced by Trichoderma koningii (koninginin A) and T.harzianum (6-penyl-apyrone) act as plant growth regulators [7]. Production of auxin (TasHyd1 from T. asperellum) after root colonization induce modification in root architecture such as increase number of root hairs and absorptive surface thereby increase nutrients up-take [8]. Qid74 from T. harzianum is involved in lateral root hair formation and elongation [4]. Trichoderma spp. can acidify their surroundings by producing organic acid [9] and these organic acids solubilize phosphates, micronutrients [10] that lead to more nutrient availability in soil. Trichoderma also produce chelating metabolites and used redox activity for solubilizing the minerals. T.harzianum is good solubilizer of plant nutrients and also reported to solubilize MnO₂, metallic zinc, and rock phosphate. Crop productivity has increased up to 30% after the addition of T.harzianum T22 and T.atroviride P1 in lettuce, tomato, pepper plants [11].

Induced Resistance

Induced systemic resistance (ISR) similar to Systemic Acquired Resistance (SAR) is activated by Trichoderma relies on signaling pathways regulated with jasonate (JA) and ethylene (ET) [12], that response to a wide spectrum of pathogens and adverse environmental conditions. About 205 proteins induced by several genes were expressed differentially in maize roots and shoots inoculated by T.harzianum T22 [13]. After invasion of Trichoderma plant that responds quickly by rapid ion fluxes and oxidative burst then accumulates the signal molecule, salicylic acid (SA) and jasmonic acid in the vascular tissue or epidermal cell of plant root [14]. PR gene function induced by this compound has coding pathogenesisrelated proteins (PR protein), secreted to inhibit pathogen infection [15]. Among variable type of PR protein, cell wall degrading enzymes like chitinase and β-1,3-glucanase are capable of lysing the cell wall of fungal plant pathogen. Trichoderma produced Xylanase and peptaibols has shown to elicit plant defense. Sm1/Epl1 are best elicitor which found an abundant amount is nothing different than cysteine-rich hydrophobin-like protein [16].

Biological Control

Parasitize and kill other fungi is apparently an ancestral trait of Trichoderma that made them successful in commercial bio-fungicides and bio-nematicides. Environmental signaling plays an important role in Trichoderma and their cell signaling is limited compared to model fungi (Neurospora crassa) but improved gradually by genetic approaches. In terms of biological control, now research focused on understanding how disease control is achieved. The combined mode of action for disease suppression of Trichoderma is stated below.

Competition for nutrients

Trichoderma has a superior capacity to mobilize and take up soil nutrients compared to other organisms. Trichoderma obtain ATP from the metabolism of different sugars by the production of different enzymes, all cellulose, glucan, chitin from environment converted as glucose used for their carbon and energy source which make them strong competitor. Limiting nutrients in rhizosphere result starvation which is the most common cause of death for other microorganisms. Eisendle et al. [17] ascribed that Iron uptake is essential for viability of filamentous fungi, and they produce siderophores (low-molecular-weight ferric-iron specific chelators) to mobilize environmental iron. Subsequently, iron from the ferri-siderophore complexes is recovered via specific uptake mechanisms. Some Trichoderma produce highly efficient siderophores that chelate iron and stop the growth of other fungi. Thus, iron availability influences the biocontrol effectiveness of Trichoderma to Pythium was evident [18].

Mycoparasitism

A number of significant studies have been conducted on the mycoparasitism of Trichoderma species with a wide range of commercially important plant pathogens and considered as more aggressive antagonist among all BCAs. The mechanism employed by Trichoderma is a complex sequential process responded with several genes, enzymes, secondary metabolites or elicitor in different species and different stages of their predation [19]. Parasitic fungi have a positive chemotrophic growth towards their host then coiling them around. Formation of apresorium take place during coiling which serve to penetrate the host and contain osmotic solutes [20]. Howell [21] also demonstrated the occurrence of coiling and formation of appresoria caused for the production of cell wall degrading enzymes and peptaibols, facilitates both the entry of Trichoderma hypha into the lumen of pathogen and the assimilation of the cell-wall content. Lytic enzymes in biological control act for over expression and deletion of there respective genes [22]. Production of cell wall degrading hydrolytic enzymes is a key step in the successful establishment of mycoparasitic relationship because cell wall is the first barrier between the fungal prey and parasite. Sequential expression of cell wall degrading enzymes, mostly chitinase, glucanase and protease (Prb1/Sp1) which regulates the remote sensing, partially in mycoparasitism [23].

Antibiosis

Antibiosis occurs during interactions involving low-molecular-weight diffusible compounds produced by Trichoderma strains that inhibit the growth of other microorganisms. Weindling [24] demonstrated a “lethal principle” excreted by T.lignorum into the surrounding medium termed as gliotoxin which kill both R. solani and Sclerotinia americana. The metabolites produced by Trichoderma are harzianic acid, tricholin, gliovirin, glisoprenins, heptelidic acid, alamethicins etc. [25]. These volatile and non-volatile toxic compounds impede colonization of pathogen. Monte [26] described the combined effect of hydrolytic enzymes and antibiotics results supreme antagonism than that of single one. Mycoparasitism by coiling of hyphae (in vitro) and enzyme-mediated antibiosis (in vivo) were the main mechanisms of biocontrol of T. harzianum against Rhizoctonia solani in sheath blight of rice which was evident by Cumagun and Ilag [27]. Wiest et al. [23] found peptaibols; another strong antimicrobial metabolite, synergistically act with cell wall degrading enzymes to inhibit fungal pathogen.

Tricho-Remediation

T. viride, T. harzianum and T. reesei being extensively studied to produce extracellular cellulolytic enzymes, namely EGs, endoglucanase, Cello biohydrolase, xylo-glucanases, Glucan endo-1,6 β glucosidase, endochitinase, xylanase and cellobiase which act synergistically in the conversion of cellulose to simple sugars like glucose. These cost-effective enzymes play the key role in the recycling of cellulose from cellulosic waste materials in biofuel and bio-refinery technologies also deployed in textile and paper industries [28]. Hazardous organic wastage including degradable municipal solid waste can be digested quickly with the enzymes cocktail thus recycling of residues increases usable energy as well as resolving the pollutions. Tricho-composting of farm accumulated crop residues is the best remedy for managing debris in short duration to nullify the bad-impact of Agricultural burning. Enzymes of Trichoderma to break the polymers of the lignocelluloses complex are potentiality reported by Michael et al. [29]. Different Trichoderma strains possess innate resistance to synthetic chemicals including herbicides, fungicides and pesticides such as DDT, contaminants at different levels [30]. Trichoderma inhamatum exhibited a remarkable capacity to reduce Cr (V1) concentration completely [31] as a result myco-remediation initiated in Cr(V1) contaminated waste water. Shukla and Vankar [32] studied biosorption by Trichoderma species and found 100% chromium up-take in a culture plate. Microorganism implies various physico-chemical interactions for metal up-taking and most understood methods are extracellular precipitation, cell surface sorption and Intracellular accumulation. Vast release of industrial effluents makes our surroundings toxic to plant and human, metal recovery and mitigation can be done by Trichoderma biosorption and enzymatic digestion in a potential manner. The fungi of interest opened-up a large premise for obtaining agricultural sustainability in adverse climate by eliminating toxicants from soil and water.

Climate Stress Reliever

Trichoderma are now studied in respect to abiotic stress and observed some of this species improve survival of plants in hostile environment by increasing plant tolerance. During fungal-plant interaction at rhizosphere, a mechanism is happen connecting to an increase in the water absorption effectiveness because of increased root architecture. Trichoderma alter the response of plant like drought avoidance through morphological adaptation, drought tolerance through physiological adaptation [33], and can also induce systemic resistance to abiotic plant stress including water deficit, salt and temperature stress. Singh et al. [34] observed in an experiment on wheat crop raised from Trichoderma treated seed can tolerate drought better than crop raised from non-treated seed due to excellent root growth and more availability of nutrients. Viterbo et al. [35] demonstrated that arabidopsis and cucumber plants treated with Trichoderma prior to salt stress imposition showed improve seed germination significantly through expression of several gene related to osmoprotection. These applications have major implication for plant agriculture because the use of beneficial-organism is eco-friendly and cost effective which will be a further contribution to environmental sustainability.

Conclusion

Hazard based agrochemicals withdrawn from European market also emphasize to research for easy alternatives on exploiting beneficial organism. Study on other beneficial microorganism to overcome the limitations of crop production s still limited. Trichoderma is a single multiplex for climate resilient Agriculture to ensure green growth. Genetic study is necessary to develop an integrated understanding of complex ‘plant – Trichoderma – pathogen – soil interaction’; in resolving program.

References

1. Kubicek CP, Bissett J, Druzhinina L, Kullnig-Gradinger C, Szakacs G. Genetic and metabolic diversity of Trichoderma: a case study on southeast Asian isolates. Fungal Genet Biol. 2003; 38(3): 310–319.   
2. Atanasova L, Druzhinina IS, Jaklitsch WM. Two hundred Trichoderma species recognized on the basis of molecular phylogeny. In: Mukherjee PK, Horwitz BA, Singh US, Mukherjee M, Schmoll M (eds). Trichoderma: Biology and Applications. U.K. CABI of Nosworthyway, Wallingford, Oxon. 2013: 10–42.   
3. Dinesh R, Prateeksha M. A review on interactions of Trichoderma with Plant and Pathogens. Research Journal of Agriculture and Forestry Sciences. 2014; 3(2): 20–23.   
4. Samolski I, Rincón AM, Pinzón LM, Viterbo A, Monte E. The qid74 gene from Trichoderma harzianum has a role in root architecture and plant bio fertilization. Microbiology. 2012; 158: 129–138.   
5. Zhang F, Yuan J, Yang X, et al. Putative Trichoderma harzianum mutant promotes cucumber growth by enhanced production of indole acetic acid and plant colonization. Plant Soil. 2012l 368: 433–444. http://dx.doi.org/10.1007/s11104-012-1519   
6. Morán-Diez E, Hermosa R, Ambrosino P, et al. The THPGI end opolygalacturonase is required for the Trichoderma harzianum-plant beneficial interection. Mol Plant Microbe Interact. 2009; 22(8): 1021–1031.   
7. Liu SD. The use of benomyl resistance mutant of Trichoderma koningii as a biocontrol agent against root rot disease of Chrysanthemum and adzuki bean Trichoderma. News Lett. 1988; 4–5.   
8. Contreras-Cornejo HA, Macias Rodriguez L, Cortés-Penagos C, López-Bucio J. Trichoderma virens, a plant beneficial fungus, enhances biomass production and promotes lateral root growth through an auxin-dependent mechanism in Arabidopsis. Plant Physiol. 2009; 149: 1579– 1592. doi: 10.1104/pp.108.130369   
9. Gómez-Alarcón G, de la Torre MA. Mechanisms of microbial corrosion on petrous materials. Microbiología. 1994; 10: 111–120.   
10. Harman GE, Howell CR, Viterbo A, Chet I, Lorito M. Trichoderma species-opportunistic, avirulent plant symbionts. Nat Rev Microbiol. 2004; 2(1): 43–56.   
11. Vinale F, Ambrosio GD, Abadi K, Scala F. Application of Trichoderma harzianum (T22) and Trichoderma atroviride (P1) as plant growth promoters, and their compatibility with copper oxychloride. J Zhejiang Univ Sci. 2004; 30: 2–8.   
12. Van der Ent S, Van Wees SCM, Pieterse CMJ. Jasmonate signalling in plant interections with resistance-inducing beneficial microbes. Phytochemistry. 2009; 70: 1581–1588.   
13. Shoresh M, Harman GE. The molecular basis of shoot responses of maize seedlings to Trichoderma harzianumT22 inoculation of the root: A proteomic approach. Plant Physiol. 2008; 147: 2147–2163.   
14. Tuzun S, Kloepper JW. Induced systemic resistance by plant growth promoting rhizobacteria. In: Ryder MH, Stephens PM, Bowen GD (eds). Improving plant productivity with rhizosphere bacteria, Proceedings of the Third International Workshop on Plant Growth Promoting Rhizobacteria. CSIRO, Australia. 1994: 104–109.   
15. Wasternack C, Stenzel I, Hause B, et al. The wound response in tomato-Role of jasmonic acid. J Plant Physiol. 2006; 163: 297–306.   
16. Druzhinina IS, Seidl-Seiboth V, Herrera-Estrella A, et al. Trichoderma—the genomics of opportunistic success. Nat Rev Microbiol. 2011; 9(10): 749–759.   
17. Eisendle M, Oberegger H, Buttinger R. Illmer P, Haas H. Biosynthesis and uptake of siderophores is controlled by the PacCmediated ambient-pH regulatory system in Aspergillus nidulans. Eukaryot Cell. 2004; 3(2): 561–563.   
18. Chet I, Inbar J. Biological control of fungal pathogens. Appl Biochem Biotechnol. 1994; 48(1): 37–43.   
19. Atanasova L, Le Corm S, Gruber S, et al. Comparative transcriptomics reveals different strategies of Trichoderma mycoparasitism. BMC Genomics. 2013; 14: 121.   
20. McIntyre M, Nielsen J, Arnau J, van der Brink H, Hansen K, Madrid S. Proceedings of the 7th European Conference on Fungal Genetics. Copenhagen, Denmark. 2004.   
21. Howell CR. Mechanisms employed by Trichoderma species in the biological control of plant diseases: the history and evolution of current concepts. Plant Dis. 2003; 87: 10. doi:10.1094/PDIS.2003.87.1.4   
22. Viterbo A, Montero M, Ramot O, et al. Expression Regulation of the Endochitinase Chit36 from Trichoderma asperellum (T.harzianum T-203)/a>. Curr Genet. 2002; 42(2): 114–122.   
23. Wiest A, Grzegorsky D, Xu BW, et al. Identification of peptaibols from Trichoderma virens and cloning of a peptaibol synthetase. J Biol Chem. 2002; 277: 20862–20868.   
24. Weindling R. Studies on a lethal principle effective in the parasitic action of Trichoderma lignorumon Rhizoctonia solani and other soil fungi. Phytopath. 1934; 24(11): 1153–1179.   
25. Vey A, Hoagland RE, Butt TM. Toxic metabolites of fungal biocontrol agents. In: Butt TM, Jackson C, Magan N (eds) Fungi as biocontrol agents: Progress, problems and potential. CAB International, Bristol. 2001: 311–346.   
26. Monte E. Understanding Trichoderma: between biotechnology and microbial ecology. Int Microbiol. 2001; 4(1): 1–4. doi: 10.1007/s101230100001   
27. Cumagun CJR, Ilag LL. Parasitism of Sclerotial Bodies of Rhizoctonia solani Kuehn by Trichoderma harzianum Rifai and Penicillium oxalicum Currie and Thom. Phil Phytopathol. 1997; 33: 17–26.   
28. Cavaco-Paulo A, Gubitz G. Catalysis and Processing. In: Cavaco-Paulo A, Gubitz G (eds). Textile Processing with Enzymes. Woodhead Publishing Ltd, England. 2003: 86–119.   
29. Michael HG, Wariish G, Khadar V. Interdependence of Enzymology and Agricultural Biotechnology. In Whitaker JR, Sonnet PE (eds). Biocatalysis in agricultural biotechnology. Washington, DC: American Chemical Society. 1989; 389: 1–9.   
30. Bolar JP, Norelli JL, Wong KW, Hayes CK, Harman GE, Aldwinckle HS. Expression of endochitinase from Trichoderma harzianumin transgenic apple increases resistance to apple scab and reduces vigor. Phytopathology. 2000; 90(1): 72–77. doi: 10.1094/PHYTO.2000.90.1.72   
31. Morales-Barrera L, Cristiani-Urbina E. Hexavalent chromium removal by a Trichoderma inhamatum fungal strain isolated from tannery effluent. Water Air Soil Pollut. 2008; 187: 327–336.   
32. Shukla D, Vankar PS. Role of Trichoderma Species in Bioremediation Process: Biosorption Studies on Hexavalent Chromium. Biotechnology and Biology of Trichoderma. 2014; 405–412. https://doi.org/10.1016/B978-0-444-59576-8.00030-8   
33. Malinowski DP, Belesky DP. Adaptation of Endophyte infected coolseason grasses to environmental stresses: mechanisms of drought and mineral stress tolerance. Crop Science. 2000; 40: 923–940.   
34. Singh US, Zaidi NW, Joshi D, et al. Trichoderma: a microbe with multifaceted activity. Annu Rev Plant Pathol. 2004; 3: 33–75.   
35. Viterbo A, Landau U, Kim S, Chernin L, Chet I. Characterization of ACC deaminase from the biocontrol and plant growth-promoting agent Trichoderma aspirellum T203. FEMS Microbial Lett. 2010; 305(1): 42–48. doi: 10.1111/j.1574-6968.2010.01910.x