Keywords

1 Introduction

Climate change, as an ongoing scenario, is already markedly interfering with agricultural productivity and food security in the world, with a gloomy scenario in the near future (Zari 2014; Daryanto et al. 2016; Naumann et al. 2018). According to a FAO report (FAO 2007), less than 5% of the entire land area of the planet has not yet been altered by human activity. Food production issues associated with abiotic stresses in plants will remain in evidence in the near future, partially driven by (i) the consequences of COVID-19’s huge impact in global economy, (ii) the necessity of reducing carbon footprint on Earth (Stern 2016), and (iii) the loss of biodiversity that will affect ecosystems and economy in an interdependent manner (Dasgupta 2008; Trisos et al. 2020; Rousseau and Deschacht 2020).

Throughout evolution, plants have accumulated mechanisms of response to various environmental factors that cause stress, allowing their adaptation to a variety of environments (Devi et al. 2017). These responses involve individually or jointly regulated signaling pathways, involving molecules such as ions, metabolites, cofactors, phytohormones, reactive oxygen species (ROS), and mitogen-activated phosphorylation cascades (MAP kinases activities) for induction of adaptive responses (Lata et al. 2018). In addition, plants make symbiotic/mutualistic interactions with rhizospheric and phyllospheric microorganisms that often result in an integrated relationship in which the roles of endophytes help induce abiotic stress tolerance for the holobiont (Lewis 1985; Marasco et al. 2012; Hardoim et al. 2015). To cope with harmful effects of abiotic stresses, microorganisms can directly synthesize anti-stress protective compounds (e.g., amino acids, glycine betaines, polyamines, amides, etc.) or act indirectly, through interfering with plant gene expression and synthesis of enzymes, hormones, and signaling proteins/molecules that activate the plant’s stress-response system soon after exposure (Schulz et al. 2002; Chakraborty et al. 2015). In addition, microbes can promote growth, which aids in the prevention of losses in plant vitality (Harman and Uphoff 2019).

The fungal genus Trichoderma stands out in the context of microbial-induced beneficial effects to plants, as it is the basis for a variety of commercially available biopesticides, biofungicides, biofertilizers, and soil conditioners (Harman et al. 2004; Vinale et al. 2008; López-Bucio et al. 2015). This is possible because this genus has several species with multiple abilities, such as antagonism to a diversity of plant pathogens, enhancement of plant defense mechanisms, and improvement of plant growth and development (Loguercio et al. 2009a; El_Komy et al. 2015; Jalali et al. 2017; Ghorbanpour et al. 2018; Lombardi et al. 2018). Another interesting characteristic that has been described for Trichoderma species is related to their contribution to the relief of abiotic stresses in plants (e.g., Xiang et al. 2012; Calvo et al. 2014). Species of this fungus display a genetic arsenal that allow the production of an array of metabolites with antifungal and antibiotic activity, as well as with bioactivities of potential pharmaceutical use (Duran et al. 2010). Some of these metabolites can also help plant hosts to cope with harmful effects of abiotic stresses (Meena et al. 2017). In this context, the multifunctional properties of Trichoderma are highly advantageous for the development of environmentally sustainable strategies for agriculture (Harman 2011a, b; Glare et al. 2012; Berg et al. 2013; Chakraborty et al. 2015; Chojnacka 2015; Kumar and Verma 2018; Lata et al. 2018).

In this chapter, we adopted a systematic/integrative evaluation of the literature to describe the use of Trichoderma spp. in the alleviation of the negative effects of abiotic stresses in plants. The methods were based on qualitative and quantitative assessments of the scientific literature according to the methods described below. The main topics analyzed were (i) temporal and geographic aspects of the selected studies, (ii) species of Trichoderma and the plants/crops involved, (iii) types of abiotic stresses, (iv) mechanisms that Trichoderma use to minimize the negative effects of abiotic stresses in plants, and (v) plant genes possibly involved in interactive mechanisms with Trichoderma that ameliorate the stresses. Application potentialities and future research directions on this issue were also addressed.

2 Overview of the Methods and Procedures

The elaboration of the questions and the research protocol (Table 1) for the systematic part of the review research in this chapter were based on five components of the method described by Kitchenham (2004): (i) population, plant species that suffer the effects of abiotic stress; (ii) intervention, Trichoderma species/isolates applications; (iii) comparison, stress-bearing plants with vs without effects from interactions with Trichoderma species; (iv) hypothesis, Trichoderma spp., on average, which reduce the negative effects caused by abiotic stresses on plants; and (v) type of study, scientific articles containing primary studies. Quantitative and qualitative data collection during the research was based, therefore, on the question of what is the magnitude of the Trichoderma species’ potential to ameliorate the negative effects caused by abiotic stresses on plants. The overall sequence of systematic steps of this chapter is described briefly as follows: the literature research was carried out using two keywords, “Trichoderma ” and “abiotic stress,” with the aid of the “Publish or Perish” version 6.2 program (P&P) (Harzing 2007) for the publications until February 2018; the Google Scholar was chosen as the main database used through the P&P program because it provides access to studies from virtually all databases and publishers available on the web. For the period of 2018–2020, the same two keywords were searched directly in the Web of Science, Scopus, and PubMed databases; this procedure aimed to provide a more representative sampling of the literature, with emphasis on the more recent research covered in the three mostly accessed databases. The initial search by P&P was performed using the two keywords above located anywhere in the full text of the publications. Since the P&P’s criterion for ranking the retrievable studies is their number of citations, which we considered as an important parameter for quality and representativeness of our sampling (Harzing 2007), the research was limited to the first 1000 studies in English retrievable by P&P. The first approach to all these retrieved studies was based on the detailed reading of the corresponding titles and abstracts to retain only those specifically dealing with the central theme of this research. From this procedure, 134 papers were selected (Fig. 1), including 71 primary studies, 30 reviews, 28 book chapters, 3 theses/dissertations, and 2 open letters. To confirm the quality and consistency of these studies, the criterion of displaying a recognized peer review system and editorial board was observed. Based on this experience, for the studies retrieved directly from the three databases indicated above for the years 2018–2020, the focus was directly on the “title” and “abstract” sections to select studies specifically related to our investigation. With this procedure, 46 primary studies were initially retrieved, and, after the analysis of the abstract contents, 19 papers were retained and added to the local database under assessment (Fig. 1).

Table 1 Research protocol for the systematic review of web-based scientific literature
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Fig. 1
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Flow diagram of the search strategy, selection of studies, and data management procedure on the role of the genus Trichoderma in generating plant tolerance to a variety of abiotic stresses

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In the next step, we applied a series of inclusion/exclusion criteria established in the protocol, so that those studies presented in the form of proceedings’ abstracts, theses, dissertations, reviews, book chapters, and open letters were removed; only the 71 research articles containing primary studies remained. For the three databases direct search, two papers were removed, leaving us with 17 studies for the next steps (Fig. 1). With all these initially selected studies, the reading of the full text was performed for data extraction and qualitative/quantitative assessments. During this process, three articles from the P&P search and five from the three databases direct searches were further removed based on lack of key information required for our research analyses (i.e., they did not meet inclusion criteria), leaving us with a final number of 68 + 12 articles (Fig. 1), in a total of 80 primary studies articles that composed the literature database used for the systematic part of this chapter (Table 2). Further validation and integration of the systematized knowledge collected were achieved by assessing related publications, through regular (classical) database search, according to specific aspects of interest suggested by the up-to-date literature obtained in the systematic review.

Table 2 Final database of articles included in the systematic review
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3 When, Where, and How Trichoderma Has Been Tested for Abiotic Stress Alleviation?

3.1 Language and Timing of the Science on Trichoderma-Plant-Abiotic Stress Interactions

Considering the most recurring words in the titles of the 1046 initial studies retrieved and in the 80 finally selected papers, and after taking the searching keywords “Trichoderma ” and “abiotic stress” away from the analyses, the words “plant(s),” “harzianum,” and “growth” (Fig. 2) were highlighted. After selection of the studies according to the established criteria (see review methods), the words related to the main types of stresses investigated became highlighted. Other frequent title words found for the 1046 studies were “tolerance,” “resistance,” “induced,” “response,” “stresses,” “gene,” and “expression,” thus referring to the interaction between Trichoderma and plants (Fig. 2a). When observing the wording of the 80 finally selected primary studies, the following groups of terms acquired more relevance: (i) “growth,” as the main response variable for plant studies of this nature; (ii) “harzianum” and “asperellum,” related to the most common Trichoderma species used in the studies; (iii) “rice” and “maize”, indicating the most tested plant species; (iv) “drought ,” “salt,” and “salinity,” as well as “cadmium” and “arsenic’ (representing metal-polluting elements), which refer to the most studied stresses; and (v) “seed(ling)” as the main part of the plant for inoculation/assessments (Fig. 2b). The word “gene” is relatively recurrent in both word clouds. These results, at a first glance, point to the trend that the research specifically dealing with abiotic stresses is focusing on those two Trichoderma species, three crops, and three types of stress, with a preferable form of inoculation.

Fig. 2
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Temporal distribution of scientific publications involving “Trichoderma ” and “abiotic stress.” The word clouds were assembled with the most repeated words in the titles of the 1046 of the total search (a) and with the 80 articles systematically selected (b) (the size of the words indicating the frequency of appearance). The time curves represent the number of publications selected; the dotted-line curve (Y-axis on the left) corresponds to the 1046 initial studies retrieved and the solid-line curve (Y-axis on the right) to the final database of 80 articles

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From a temporal standpoint, research on Trichoderma , beyond their use as biocontrol agents against phytopathogens, began to grow exponentially from 2006 onward (Fig. 2), likely due to, at least in part, an increased consciousness of the negative consequences of global warming and climate changes for sustainable agriculture. It is worth to highlight the years of 2014, followed by 2017, in which more studies were published. The number of articles on Trichoderma in general began to increase in the 2000s, roughly coinciding with the raise in the number of commercially available bioproducts (Waghunde et al. 2016). Since 2014, there are already more than 250 registered bioproducts in the world that are based on Trichoderma species, either individually or in combinations (Woo et al. 2014), which correspond to around 60% of the world’s biofungicide market. Trichoderma harzianum comprises ~83% of these products (Topolovec-Pintarić 2019) and also corresponds to one of the most recurrent words in the recovered studies (Fig. 2b). Bioproducts represent a small share of the plant-protection market, mainly due to their slow activity and dependence on environmental factors, which has been seen as a constraint to their effectiveness in the field (Singh et al. 2018); further issues related to difficulties and costs of registration add to this context (Topolovec-Pintarić 2019). However, the reported increase in their utilization likely reflects the current demand for healthier foods, free from chemical residues (Gomiero 2018). The use of Trichoderma as biofertilizers to improve plant growth has facilitated registration, thereby increasing its availability in the market (Topolovec-Pintarić 2019). It is noteworthy that the potential of offering bioproducts at lower costs for smallholders to deal with their production necessities can assist with food security globally (Harman 2011b).

3.2 Geographic Distribution of Studies with Trichoderma and Abiotic Stresses in Plants

To assess whether there was any geographical tendency for studies of this nature, the articles systematically retrieved were distributed as indicated on the map (Fig. 3), and the type of experiment performed was also registered. The 80 selected studies were performed in 19 countries, where 67.5% were from Asia, followed by countries from Europe and the Americas (15 and 11.25% respectively), and from Africa (6.25%). The significant number of studies in Asia was due to India’s outstanding contribution (30% of total articles), followed by China (16.25%). This is consistent with the fact that India contributes to ~90% of Asian market of Trichoderma-based products (Woo et al. 2014; Singh et al. 2018). From the selected publications, 74.1% of the studies were performed in greenhouses and growth chamber (90% and 10%, respectively), 17.3% in fully controlled environments (in vitro), and 8.6% under field conditions (Fig. 3).

Fig. 3
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Geographic distribution and types of experiments for the systematically selected primary studies of our search

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India and China have their economies composed by agriculture as an important component (Foley et al. 2011), combined with a very strong and consistent industrial development allied to high population counts. These circumstances tend to be associated with issues such as environmental degradation and pollution (Ballescá 2016; Chopra 2016), especially by heavy metals (Sodango et al. 2018). Furthermore, human population growth, urbanization, and climate changes are further challenges to be faced, in order to cope with food production in an environmentally sustainable way (Foley et al. 2011; Du et al. 2018). All these issues must be dealt properly to assure global food security (Godfray et al. 2010; He et al. 2013). It has been proposed that investments in agronomic research and development toward sustainable strategies and products (e.g., Trichoderma-based bioproducts) can not only help solving those challenges but also stimulate agricultural productivity on a long-term scale (Heisey and Fuglie 2018).

3.3 Trichoderma Species, Their Origin, Targeted Plants, and Inoculation Methods

A total of 175 Trichoderma isolates were associated with abiotic stresses in the selected studies, with 78.9% distributed in 16 species and the remaining not identified to the species level (Fig. 4a). As indicated by the word clouds (Fig. 2b), T. harzianum and T. asperellum were the most abundant species, with 75 and 21 isolates, respectively, within the 138 isolates that were identified up to the species level. The other species all together occurred in a frequency of 30.4%: T. longibrachiatum with eight; T. atroviride with six; T. afroharzianum and T. britannicum with five isolates each; T. virens with four; T. parareesei with three; T. asperelloides , T. hamatum , and T. reesei with two isolates each; and T. aggressivum , T. koningiopsis , T. simmonsii , T. saturnisporum , and T. viride with one representative each (Fig. 4a). The data obtained on the sources of these isolates indicated that most came from collections of the study-affiliated or collaborating institutions (38.3%) or from rhizospheric soil (28.6%, Fig. 4a). Considering only isolates from collections’ material, 55.2% were T. harzianum . When collection isolates were not taken into account, 72.2% of the isolates were from soil. Isolates from contaminated environments (mining tailings and contaminated soil) were specifically tested against stresses caused by heavy metals. Only in four studies, Trichoderma species (T. harzianum , T. asperellum , and T. atroviride ) were used as formulated bioproducts, which were then tested for their effects on plant responses to abiotic stresses (Fig. 4a). In general, data suggest that the observed roles of Trichoderma in abiotic stress relief come from research primarily aimed at complementing the current knowledge on activities, applications, and bioproducts’ development of particular isolates, most of them already known as biocontrol agents (e.g., Woo et al. 2014; Waghunde et al. 2016; Anam et al. 2019). Since only a small proportion of different Trichoderma species/isolates have been studied as mitigators of abiotic stresses (Fig. 4), there is still much exploration to be done, given the large diversity found in this genus worldwide (De Souza et al. 2006; Loguercio et al. 2009a; Kubicek et al. 2011; Feitosa et al. 2019).

Fig. 4
figure 4

Distribution of Trichoderma species and sources, inoculation methods, and host plants. (a) The sources of Trichoderma isolates for the reported studies are shown in the X-axis; the taxonomic definition found for the experimental isolates within the 80 articles is appearing in the center of the graph. All isolates in which their species were not defined are collectively represented by “Trichoderma spp.” (b) Plant species used in the experiments as targets for the applied stresses and inoculated with the Trichoderma isolates; distribution of the modes of inoculation appear in the center of the graph. The total number of studies considered (86) exceeded the 80 systematically selected articles, as in some of them , there was more than a single type of study/experiment being reported

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The most frequent plant species found in the selected studies were maize (Zea mays , 12.8%), rice (Oryza sativa , 11.6%), tomato (Solanum lycopersicum , 10.5%), Arabidopsis thaliana (9.3%), and wheat (Triticum aestivum , 8.1%) (Fig. 4b; also see Fig. 2). Among the methods used to inoculate Trichoderma , seed biopriming alone (i.e., soaking seeds with suspensions of fungal spores to allow seed germination before planting) was the most used (Fig. 4b). Trichoderma spore suspensions directly applied into the soil (liquid or powder) or on the roots (by spraying) corresponded to 44.2% of the studies. Other inoculation methods, including mycelium discs for volatile compounds experiments and in vitro techniques, as well as inoculation of flowers and leaf tissues comprised the remaining 17.5% (Fig. 4b). These three predominant inoculation methods correspond to those usually planned for and used in large-scale crop applications, mainly for the most studied plant species (Fig. 4b), which combine ease of product manipulation and delivery with lower costs (Parnell et al. 2016; Rocha et al. 2019).

Trichoderma is one of the most abundant and widespread fungal genus in the world and has characteristics that justify the amount and depth of studies on them (e.g., reviews by Harman et al. 2004; Vinale et al. 2008; Schuster and Schmoll 2010; López-Bucio et al. 2015). Trichoderma spp. can adapt to a diversity of environments, not only due to their ability to sporulate in response to a complex and intertwined variety of environmental factors (Loguercio et al. 2009b; Steyaert et al. 2010a, b, c) but also due to a phylogenetic and genome-printed high opportunism (Druzhinina et al. 2011) that allow the occupation of a broad array of niches and environmental gradients (Mukherjee et al. 2013; Egidi et al. 2019; Jiao and Lu 2020). The production of a variety of hydrolytic enzymes (e.g., reviewed by Schuster and Schmoll 2010; Mukherjee et al. 2013; Waghunde et al. 2016), a great ability to control cell-wall synthesis and repair in themselves and in their hosts (Gruber and Seidl-Seiboth 2012; Kappel et al. 2020), and some tolerance of certain isolates to higher temperatures (>32 °C) during growth (Chang et al. 1997) certainly contribute to this wide niche occupancy (including a great variety of plant hosts). Some species have an endophytic lifestyle, colonizing plants by penetrating root cells and remaining throughout the plant life cycle (Harman et al. 2004, 2019; Contreras-Cornejo et al. 2018). Trichoderma harzianum is the most used species in bioproducts and in experiments to control plant pathogens and the one most commonly found in soil environments (Vinale et al. 2008; Mukherjee et al. 2013; Woo et al. 2014; Waghunde et al. 2016), which explains why it is the species most frequently found in this review (Fig. 4a). Since T. harzianum is a species complex, with multiple cryptic species, i.e., a complex group of morphologically indistinguishable species (Chaverri et al. 2015), this is likely another reason for its higher frequency in the systematically retrieved studies dealing with abiotic stress relief in plants. Trichoderma spp. are predominantly saprophytic fungi in soil, litter, organic matter, and rhizospheric ecosystem of all climatic zones, and their diverse metabolic capacity allows them to colonize soils of different habitats (Vinale et al. 2008; Druzhinina et al. 2011; Mukherjee et al. 2013). It is such a strong competitive nature of these fungal species that provide rapid rhizospheric establishment, root colonization (including interaction with arbuscular mycorrhizal fungi; Mehta and Sirari 2019), pathogenic microflora control, and plant-growth promotion (Hidangmayum et al. 2018). These characteristics, therefore, allow to explain their frequent interaction with the surface of plant roots, so that strategies of isolation (or inoculation) of these isolates tend to be often related to forest or agricultural soils and seed coating/biopriming (Topolovec-Pintarić 2019; Rocha et al. 2019) (Fig. 4).

The experimental plants used for the interactive experiments with Trichoderma tend to be mainly crop species that are mostly recognized as displaying short life cycles, small sizes, easy propagation, and considerable economic importance, being well-established model plants for a great variety of research in plant biology and agricultural sciences (Fig. 4b). Moreover, the high frequency of inoculation methods involving seeds and/or soil (~3/4) suggests a natural overlap between basic/applied research and technological development of methods/products for agricultural applications. The biopriming of seeds with Trichoderma spp. has been used to improve seedling vigor, which can be triggered by the release and/or production of enzymes and phytohormones involved in seed viability and germination rates and speed (Kumar et al. 2014; Babychan and Simon 2017), as well as in resistance against pathogens (Mastouri et al. 2010; Singh et al. 2019, 2020). With Trichoderma inoculation in roots/soil, additional features occur such as alteration of soil microflora and increase of nutrients availability, due to degradation of many complex substrates. Currently, the use of changing microbial communities of cultivated soils and improvement of the performance and vigor have been widely used in agricultural production (Harman and Uphoff 2019).

4 Types of Abiotic Stresses in Plants Alleviated by Trichoderma

From the 80 final articles selected, 105 abiotic stresses were identified, which were classified into 13 groups (Fig. 5). The highest proportion of the studied stresses were saline stress (36.2%), agreeing with the word clouds (Fig. 2); within this fraction, 92.7% corresponded to the effects of the salts as a single factor, with the remaining three studies (7.3%) assessing this factor in combination with high temperature and osmotic and alkaline stresses (one study each) (Fig. 5). Drought stress was the second most represented (27.6%), with water deficit being analyzed in combination with heat stress in one study (Fig. 5). Stresses caused by heavy metals comprised 21% of the studies retrieved. These 22 studies included 7 chemical elements and were distributed as follows: arsenic (six), cadmium (five), lead (four), copper (three), zinc (two), and chromium and nickel (one each) (Fig. 5). Taken together, these three types of abiotic stress comprised 83.8% of the experiments involving Trichoderma isolates and plants.

Fig. 5
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Types of abiotic stresses in plants alleviated by Trichoderma . Twelve different types of abiotic stresses (single or in combination) were found in the selected studies (left-side graph). The number of studies reporting stresses caused by heavy metals were discriminated by each metal (right-side graph). Thermal stress was further divided (proportionally) into high and low temperatures

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Under the circumstances of climate change, salinity and drought can be viewed as the most relevant types of abiotic stress that can affect crop production (Munns and Gilliham 2015); moreover, they are interconnected not only due to their direct relationship with water availability (Nuccio et al. 2018) but also through their effects in the osmotic balance and regulation in plant cells (Mastouri et al. 2010; Ikram et al. 2019; Poveda 2020). From this standpoint, our analysis indicated that ~2/3 of the current science on Trichoderma-mediated abiotic stress relief deals with the physiological and/or biochemical responses of plants toward osmoregulation and water use efficiency (Munns and Gilliham 2015; Ikram et al. 2019; Khoshmanzar et al. 2020), which are major issues expected to affect plant survival, growth, and productivity in a climate change context (Daryanto et al. 2016; Naumann et al. 2018; Khoshmanzar et al. 2020).

By disrupting osmotic equilibrium, saline stress alters membrane stability, increases the toxicity of ions within the plant cells, and affects photosynthetic rates (Khomari and Davari 2017; Meena et al. 2017; Mona et al. 2017; Ikram et al. 2019). Due to the lower availability of water created by a higher osmotic pressure (an effect similar to that caused by drought ), the plants tend to respond physiologically to these stresses as if they were in a process of acclimation (Farooq et al. 2009; Filippou et al. 2013). The stress induces changes in membrane function, which tends to disrupt the ionic phase, so that cell toxicity results from accumulation of ions, which causes oxidative stress and biochemical imbalances (Begum et al. 2019); depending on their intensity, duration, and speed, these changes can lead to either acclimation or apoptosis (Filippou et al. 2013; Yang and Guo 2018). Furthermore, plants under drought conditions suffer from water supply limitations both by the root system and from the transpiration losses (Tardieu et al. 2018), although a decrease in transpiration rates is a major plant response to this stress (Farooq et al. 2009). The consequent decrease in water potential interferes with the photosynthetic process, by affecting the stomatal opening/conductance, much as a result of responsive-hormones synthesis, as well as of changes in the chlorophyll and carotenoid contents (Mona et al. 2017; Begum et al. 2019). In terms of cellular processes, these water-deficit stresses affect cell division, cell-wall dynamics, primary and secondary metabolism, regulation of hormones and synthesis, and accumulation of reactive oxygen species (ROS) (Bray 2007; Takahashi et al. 2018; Tardieu et al. 2018; Zhang et al. 2019a, b). Reduction in size of leaves and seeds, root growth suppression, and flowering/fruiting delays are additional stressing effects at morphological and physiological levels (Mastouri et al. 2012; Osakabe et al. 2014). Since all of these effects ultimately lead to decrease in plant growth and productivity, Trichoderma treatments appear as a relevant option (Mona et al. 2017; Ikram et al. 2019; Zhang et al. 2019a; Poveda 2020) for the development of salt- and drought-tolerance to cope with those additional types of stresses (Farooq et al. 2009; Filippou et al. 2013).

The next most recurrent stress in the studies was caused by heavy metals (Fig. 5). Trichoderma spp. applications have shown to be promising alternatives for amelioration of this stress, either alone or combined with salinity. Interestingly, such conditions allow improved phytoremediation activities for plants in metal-polluted soils (Anam et al. 2019; Li et al. 2019). In general, the presence of these metals in soil can affect plants in a variety of forms, such as reducing seed germination, chlorophyll contents, photosynthesis, and ATP synthesis; altering water balance, nutrient absorption by roots, mitochondrial and chloroplast activities, cell signaling, and enzymatic activities; and increasing membrane lipid peroxidation, levels of ROS , etc. (Ghori et al. 2019; Arif et al. 2019). Usually, all these disturbances can lead to a net effect of decreasing and/or halting plant growth and to necrosis of parts or the whole plant (Groppa et al. 2007). Soil, water, air, and trophic chain pollution is mainly caused by anthropic actions of industrial (power and heat, metallurgy, steel-making, leather, paper, textile, electroplating, electronics, petrochemistry, waste and landfills, etc.), agricultural (chemical fertilizers and pesticides, sewage irrigation), mining (coal, crude oil, iron, and other metals), and urban life (He et al. 2013; Hu et al. 2014; Etesami 2018). For instance, due to the large and strong industrial, urban, and rural development of the last decades in densely populated regions, India and China have shown one of the highest levels of soils, water, and air contamination by heavy metals in the world (Hu et al. 2014; Paul 2017; Mukherjee et al. 2020), especially in rural areas, which have been generating much concern about food security and human health (He et al. 2013; Huang et al. 2018; Yang et al. 2018). Hence, these circumstances also help explaining the highest proportion of studies found for these two countries (Fig. 3).

5 Parameters Evaluated in the Studies of Trichoderma-Plant-Abiotic Stresses

The most assessed variables in studies with plant-Trichoderma-abiotic stress interactions can be classified as indirect or direct responses: in the former group, the final phenotypic effects (i.e., plants growth and development) are evaluated, whereas in the latter, biochemical/cellular pathways and compounds related to physiological and photosynthetic processes are gauged (Table 3). To act on recovery and/or amelioration of the adverse effects that the abiotic stresses cause in plants, Trichoderma spp. interfere in the physiology, biochemistry, and morphology of the host through the diverse genetic and metabolic arsenal available in this fungal genus. The quantification of relief effects of abiotic stresses in plants by Trichoderma has been studied by an array of response variables, which, in some cases, can link to possible mechanisms of action. These parameters are related to physiological, morphological, physical, and (bio)chemical aspects, which could be classified into four main categories by conceptual affinity (Table 3; Fig. 6).

Table 3 Parameters used to study mechanisms possibly involved in the alleviation of abiotic stresses in plants by Trichoderma a
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Fig. 6
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Possible mechanisms involved in the interaction between Trichoderma and plants in response to abiotic stresses. The information retrieved on genetic products in this figure refers to 13 articles in which studies of gene expression were found. Different colors represent four main groups of activities/functions identified for the plant genes involved in stress mitigation: blue, transcription factors; pink, metabolic pathways; green, signal transduction; orange, structural proteins and protective compounds . The symbols located on the left inside the balloons represent gene expression modulation in relation to treatment Trichoderma-plant-stress vs plant-stress only: ▲ green, upregulation of gene expression; ▼red, downregulation in gene expression; ‘=’ expression level without significant difference; ‘*’ transgenic plants expressing Trichoderma genes

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5.1 Influence of Trichoderma on Plant Growth and Development

Out of the 485 experiments found in the 80 systematically selected articles whose data was collected (Table 3), the most frequent group of variables were growth and development parameters (35.7%), mainly root and shoot biomasses (fresh and dry length and weight), which are measures of plant vitality as evidence of their recovery from stresses. Taking the results of Trichoderma application into account, the overall positive effects on plant growth and development could be observed, with increases in relation to control treatments varying from 77.7% improvement in the number of leaves to 4457.7% raise in root dry weight (Table 3).

Another relevant group of parameters evaluated in addressing Trichoderma effects on plant stresses was more specifically related to plant physiology, mostly focusing on photosynthesis and represented 19.2% of the variables evaluated in this study (group # 2, Table 3). Photosynthetic efficiency reflects growth, development, and biomass production, and it was assessed in the studies on saline and drought stresses (56% and 25.8%, respectively).

All Trichoderma species are mycoparasites, having thus developed a diversified and unusual biosynthetic machinery, including metabolites acting both on antagonism and survival (Druzhinina et al. 2011; Kubicek et al. 2011). As a consequence of such a metabolic variety, members of the Trichoderma genus can reduce the concentration of toxic substances in the soil, solubilize phosphates and micronutrients, synthesize siderophores, increase nitrogen fixation, and produce plant hormones (Mukherjee et al. 2013; Hidangmayum et al. 2018; Lombardi et al. 2018). Rhizospheric and endophytic Trichoderma have been reported to help host plants to adapt to abiotic stress conditions and promote their growth also through biosynthetic pathways of plant hormones (Yan et al. 2019), as well as through a variety of secondary metabolites synthesized, which aid in the solubilization of mineral compounds that increase availability of nutrients and so nutritional uptake and root growth (Rajput et al. 2019).

5.2 Alleviation of Oxidative Stresses by Trichoderma

The other two categories of variables addressed in experiments with Trichoderma were represented in our dataset as follows: 24.1% for variables related to enzyme activities and cellular functions directly affected by the stresses and 21% for levels and rates of compounds synthesized as responses to the stresses (Table 3). Within the group of variables gauging activities directly related to stress responses (group # 3, Table 3), almost the totality of the retrieved studies deals with either antioxidant activities (65%) or membrane/lipid effects (33.3%). Within the antioxidant enzyme activities related to oxidative stress response/regulation, superoxide dismutase (SOD), catalase (CAT), peroxidase (POD), ascorbate peroxidase (APX), and glutathione reductase (GR) and peroxidase (GPX) were the most prominent found (Table 3). In terms of membrane-related studies, the most prevalent specific activities were lipid peroxidation (with special interest in the use of malondialdehyde), which made up 51.2% of the analyses in this subgroup (Table 3). The composition and stability of the plasma membrane, which was used to test stress damage levels to plant cells, made up 28.2% of the studies, and the remaining four assessments dealt with electrolytic leak and translocation factors (two studies each).

The parameters relating to the content of certain substances synthesized by plants (Table 3, group # 4) were grouped as such because they are indicators of, or relate to stress states, or yet belong in metabolisms or processes that assist in physiological recovery from the action of abiotic stresses. As a result from the higher concentration of studies in saline/drought stresses (Fig. 5), the highest frequency of studies in this category # 4 (Table 3) were related to proline levels (22.5%), which corresponded 62.5% of the studies with saline stress and 20.8% of the studies on drought tolerance (Fig. 5). Among the compounds identified in the systematically retrieved studies, there was a focus on secondary metabolites related to stress responses, such as ROS (17.6%), phenolics (10.7%), and phytohormones (7.8%). Ions and heavy metal contents also appeared well represented (9.8 and 8.8%, respectively), as some of the research was focused on this type of abiotic stress (Fig. 5).

As much as biotic factors (e.g., fungal diseases, herbivory, etc.), stressing factors of abiotic nature also cause the overproduction of reactive oxygen species (ROS) in plants, which lead to metabolic toxicity, damage to the membranes, inhibition of photosynthetic apparatus and steps, and changes in hormonal levels, among others (Selvakumar et al. 2012). The major ROS species formed (superoxide, O2–, hydroxyl, OH–, and hydrogen peroxide, H2O2) react chemically with virtually all metabolites of the plants, including proteins, lipids, and nucleic acids (Nath et al. 2013; Harman et al. 2019). As in low concentrations, ROS act as signaling molecules, with specific signatures of their steady-state levels, depending on the type of cell of the plant (Choudhury et al. 2017). The regulation of ROS levels is very precise in plant cells, being related to a fine-tuned balance between their perception and detoxification, and the redox state of the cell, with a particular relevance for chloroplasts in this metabolism (Farooq et al. 2009; Meyer et al. 2020). In this context, antioxidant compounds and enzymes act coordinately on the fine modulation of these mechanisms (Mittler 2002). Trichoderma spp. have shown to also depend on ROS signaling for a variety of their own cellular processes and responses to environmental cues (Cruz-Magalhães et al. 2019), thereby having a clear modulatory interference in plants, when interacting with them.

The majority of the studies on abiotic stresses involving plants and Trichoderma have shown to focus on drought /salinity (Fig. 5). Knowledge generated in this aspect indicates that major protection of plant cells against these stresses occurs by the promotion of osmolites’ synthesis or accumulation, which increases both the water absorption and retention capacity of the cells and the activities of enzymatic and non-enzymatic antioxidants (Hameed et al. 2014; Waghunde et al. 2016; Pachauri et al. 2019). A recurrent mechanism of action found in the studies with Trichoderma spp. was the production and accumulation of proline, an amino acid that acts as cellular osmoprotector (Harman et al. 2019), mostly in three ways: (i) by protecting intracellular macromolecules against reactive oxygen species (ROS) attack, (ii) by serving as a source of carbon and nitrogen for the cell as a result of its oxidative metabolism, and (iii), as discussed above, by acting as a modulator of the osmotic balance of the cell (Christgen and Becker 2019). Some underlying mechanisms of exogenous phytohormones production by Trichoderma , such as similar forms of abscisic acid (ABA), can also protect the plant from oxidative damage (Bano et al. 2012; Khan et al. 2015), as well as modulate other stress-response metabolisms. Members of the Trichoderma genus are outstanding producers of secondary metabolites with functions already known (Table 3, Fig. 6), although many of such compounds are still unknown. There are more than 2000 natural products, such as peptaibols, non-ribosomal peptides, polypeptide, terpenes, and steroids produced by Trichoderma ssp., which play important roles in their interaction with plants (Mukherjee et al. 2012). As mentioned above, Trichoderma species throughout evolution have developed the ability to produce a large amount of extracellular enzymes and secondary metabolites (Mukherjee et al. 2012; Kubicek et al. 2019), as well as very effective systems of resistance and repair of cellular and molecular damages (Duran et al. 2010; Ghorbanpour et al. 2018), a capability that can extend the protection to their hosts (Harman et al. 2019).

6 Plant Genes Influenced by Trichoderma in Response to Abiotic Stresses

6.1 Outline of the Studies

The analytical review of this chapter allowed us to provide a glance on the current status of research on genes and their products that can be related to the beneficial fungus-host interaction in response to abiotic stresses. Out of the systematically assembled database, about 26.3% of its articles were identified as comprising studies of this nature, dealing with in vivo biochemical and molecular methods; all the data we found on gene expression patterns related to Trichoderma-plant-stress interaction were related to plant genes (Table 3; Fig. 6), and all of them were previously known to be involved in plant stress responses and in the transport of macro and micronutrients. The largest amounts of these studies were on drought (33.3%) and saline stresses (28.6%); of the remainder, 9.5% by heavy metals evaluated stress by high temperature, low temperature, nutritional deficit, and waterlogging with 4.8% each, and 9.5% gauged combined stresses (drought + high temperature and salinity + osmotic stress). The species of Trichoderma used in these molecular genetics’ studies were T. harzianum (seven), T. parareesei (six) T. britannicum (three), T. asperelloides , and T. longibrachiatum (two each); T. afroharzianum , T. asperellum , T. hamatum , T. virens , and T. reesei (one each); and a study in which there was no identification at the species level. The plant species investigated in these studies were Arabidopsis thaliana , Brassica napus , Solanum lycopersicum , Nicotiana tabacum , Cicer arietinum , Oryza sativa , Populus bolleana, Triticum aestivum , Theobroma cacao, Zea mays , and Vitis vinifera . The studies on stress-responsive genetic expression reported the majority of the genes (77.2%) as being upregulated as the result of stress, both in the above- and belowground parts of the plants (Fig. 6). It is important to mention that 23.8% of these studies were performed with transgenic plants, in which overexpression of Trichoderma-derived transgenes (supposedly induced in the fungus as a response to some abiotic stress) were investigated on their effects in modulating plant gene expression in response to the abiotic stresses (e.g., Meena and Swapnil 2019; Mota et al. 2019).

The studies selected concerning the molecular aspects of the stress alleviation mechanisms of plants by Trichoderma were sufficiently consistent with the physiological characteristics of the assessed plants under abiotic stress conditions (Table 3). Essentially, there were four major groups of activities identified for the plant genes involved in stress mitigation: (i) transcription factors (TFs) directly involved in stress-response gene expression modulation, (ii) genes responsive to metabolism and oxidative stresses, (iii) signal-transduction pathways, and (iv) synthesis of structural/protective proteins and compounds (Table 4; Fig. 6).

Table 4 Identification of plant genes from the systematically retrieved studies
Full size table

6.2 Transcription Factors

With regard to the genes encoding TFs, studies related to their expression altered in response to the Trichoderma-plant-stress interaction showed a tendency of them to refer mostly to hormonal and pathogen-related signaling pathways and dehydration-responsive genes; they were nac1/nac6 (Ghorbanpour et al. 2018; Singh et al. 2019); dreb (dehydration-responsive element binding proteins, Brotman et al. 2013; Pandey et al. 2016; Rubio et al. 2017; Singh et al. 2020b); zfp and p13 (zinc-finger domain factors related to transcriptional repression, Bae et al. 2009); erf (ethylene-responsive factor, Roatti et al. 2013; Elkelish et al. 2020; Poveda 2020); npr1, are, areb2, arf (TFs related to salicylic acid, ABA, and auxin signaling pathways, Rubio et al. 2017; Singh et al. 2019; Elkelish et al. 2020); iaa13, myb15, myb51, wrky33 (TFs related to secondary metabolites synthesis, auxin , jasmonate/salicylate signaling pathways, Brotman et al. 2013); iro2 (iron-regulated transcription factor, Singh et al. 2019). Interestingly, recent full-genome comparisons have shown the class of transcription factors genes as one of the most abundant in the core genome of Trichoderma (Kubicek et al. 2019).

6.3 Plant Genes Responsive to Oxidative Stresses

Another relevant biological function identified for the studied plant genes was associated with pathways of direct response to stresses and to metabolic changes resulting from the stress effects (Fig. 6). The genes within this category included p5cs (encoding pyrrolin-5-carboxylate synthetase enzyme, which catalyzes a rate-limiting step reaction of proline synthesis, Ghorbanpour et al. 2018); methyltransferase and alcohol dehydrogenase (Brotman et al. 2013; Ma et al. 2020; Elkelish et al. 2020); chit3 and pr-2 (acid endochitinase and pathogenesis-related type 2 protein , i.e., beta-1,3-glucanase) (Roatti et al. 2013); acc deaminase and oxidase (Zhang et al. 2016a; Zhang et al. 2019a; Elkelish et al. 2020; Poveda 2020;); small subunit of Rubisco complex (catalyzes the limiting step of CO2 fixation), cellulose synthase, lipoxygenase (oxylipin synthesis), phosphatase involved in the last step of trehalose synthesis, invertase involved sucrose hydrolysis, and nitrate/ferredoxin-nitrite reductase (Bae et al. 2009; Roatti et al. 2013; Singh et al. 2019); and genes/enzymes involved in ROS metabolism, such as nadph oxidase 1, dehydroascorbate reductases, gst (glutathione transferase ), and all those genes encoding the antioxidant enzymes indicated in Table 3 (Montero-Barrientos et al. 2010; Dixit et al. 2011; Mastouri et al. 2012; Brotman et al. 2013; Rubio et al. 2017; Tripathi et al. 2017; Zhang et al. 2019a, b; Elkelish et al. 2020; Singh et al. 2020).

6.4 Signal Transduction Pathways

The third group of genes identified as having their expression altered as a function of abiotic stress effects was related to signaling proteins involved in stress-response physiology of plants (Table 4; Fig. 6). This group comprises the following genes/proteins: sos1 (signal protein of the salt overly sensitive pathway, Montero-Barrientos et al. 2010; Rubio et al. 2017; Zhang et al. 2019a); hk, rpk, mapk3, and 4, stk (histidine, receptor protein , MAP, and serine/threonine kinases), sen1 (senescence associated), pp2c (phosphatase protein 2C, possibly related to ABA pathway), and sot (sorbitol transporter) (Bae et al. 2009); ein2 (ethylene-insensitive protein , central to this hormone signaling pathway, Rubio et al. 2017); pyl4 (abscisic acid receptor – required for ABA-mediated responses, Poveda 2020); cbl1 (calcineurin B-like 1 protein , sensor of calcium levels, interacting/regulating a family of kinases located in endomembranes) and ugt74e2 (UDP-glycosyltransferase 74E2, related to signaling of drought stress and auxin homeostase, Brotman et al. 2013); kel1 (encodes a protein with 5 repeated Kelch-like domains, characteristic of gene families involved in cell morphology and protein-protein interactions, Hermosa et al. 2011); and tgw6 (Trafficking protein particle complex subunit, Zhang et al. 2019a).

6.5 Genes Involved in Transport and Protection Against Abiotic Stresses

Finally, the last group of stress-responsive plant genes are those encoding proteins with either a directly protective activity to ameliorate the effects of the stressing agent or a transporting activity for molecules and substances used for this protection (Table 4; Fig. 6). In the former subgroup, we found tas14 (dehydratorine of group 2 late embryogenesis abundant proteins, Ghorbanpour et al. 2018) and dhn (dehydrin, cellular protection against dehydration, also a LEA protein , Pandey et al. 2016; Singh et al. 2020b); hsp70, -4, -19 -90 (heat shock chaperones, Monteiro-Barrientos et al. 2010; Roatti et al. 2013); and osm1 (osmotic stress-sensitive mutant, belonging in the superfamily of SNARE proteins involved in vesicle/membrane fusion, Roatti et al. 2013). In the second subgroup of genes/proteins with transporting activity, there were Aqgp, aqu, tip, p31, pip1 (aquaporin-type transmembrane proteins, Bae et al. 2009; Pandey et al. 2016; Vieira et al. 2017; Elkelish et al. 2020; Singh et al. 2020b); abc and pr-5 (ATP-binding transporters) and pathogenesis-related type 5, i.e., osmotin-like membrane located protein (Bae et al. 2009); aap6 (amino acid permease 6, transmembrane transporters, Brotman et al. 2013); and Ysl15, irt1, nrt, nramp, sut2, pht/pt, amt (macro and micronutrient transporters, Singh et al. 2019).

The assessment of expression modulation of genes investigated in the Trichoderma-plant-abiotic stress interaction suggest an interplay of a variety of cellular and physiological mechanisms, many with a cross talk among signaling and metabolic pathways responsive to both biotic and abiotic stresses (Choudhury et al. 2017; Mendoza-Mendoza et al. 2018; Meyer et al. 2020). Plants have to deal simultaneously with multiple environmental stress-related cues, thus displaying a complex integration of stimuli and defense signals. Prioritizing certain physiological responses is a fine-tuned regulation resulting from plant-microbe interactions, whose understanding will be advantageous for crop improvements (Schenk et al. 2012). Further studies supported by the multi-omics, high-throughput, and comparative genomics approaches can unravel structural and functional aspects of these complex regulatory networks with unprecedent detail (Zeilinger et al. 2016; Meena et al. 2017; Kubicek et al. 2019; Arif et al. 2019), thereby providing additional opportunities for biotechnological development of Trichoderma-based bioproducts directed toward mitigation of plant stresses caused by abiotic factors (Waghunde et al. 2017; Szczałba et al. 2019; Topolovec-Pintarić 2019).

7 Conclusions and Perspectives

Environmental degradation imperils quality of life on Earth, and bioeconomy is a recent view that may properly handle the threatening circumstances. Bioeconomy has been developed on the basis of three visions – bio-ecology, bio-resources, and bio-technology (Bugge et al. 2016). In this regard, a vast array of studies on Trichoderma spp. have been widely reported in the literature, mostly due to their efficiency as biological control agents of plant pathogens, direct plant growth promotion, and the synthesis of a diverse of compounds with industrial applications (Vinale et al. 2008; Schuster and Schmoll 2010; Mukherjee et al. 2013). Nevertheless, from the beginning of this century, researchers have been pointing out that this fungal genus is even more multifaceted and so with an increasing potential for a wider diversity of applications akin to the bioeconomy view.

In this chapter, we systematically reviewed and discussed the use of Trichoderma to mitigate the negative effects of abiotic stresses on plants and discussed the consequences and potential applications of these findings, including areas of knowledge with strengths and gaps in this theme. An up-to-date sampling of articles containing primary studies reported in journals relevant to the areas of biological control, mycology, bioprospection, biotechnology development, and bioproducts were gathered, with their data being collected and assessed in details in this chapter. With specific tools, it was possible to prioritize the retrieval of more highly cited publications, which helped us to work with an amount of representative research of quality in this field (Figs. 1 and 2). Our survey was able to retrieve interesting information on the current status of research with Trichoderma , their interaction with plants, and the mitigation of abiotic stresses (Figs. 3, 4, 5 and 6).

Trichoderma of various species are commonly used as biocontrol agents and/or growth promoters, making up about 3/5 of the biofungicide market in the world (Topolovec-Pintarić 2019); since a multifunctional characteristic can add value to bioproducts, Trichoderma isolates with additional phenotypes of abiotic stress-relief for plants (Zhang et al. 2016a; Anam et al. 2019; Szczałba et al. 2019; Poveda 2020) can provide a very advantageous benefits/costs relationship for environmentally sustainable food production strategies (Harman 2011a). In a region with various environmental degradation issues to solve (Chopra 2016), India is an example of a country taking robust steps in this direction, with a significant contribution not only on Trichoderma spp. science but also on their bioproducts’ market (Woo et al. 2014). Despite having more than 300 species already described in this genus (Kubicek et al. 2019), and also a great fraction of functional isolates not yet characterized up to species level, more than 3/4 of the studies involving Trichoderma-plant-abiotic stress interactions have appeared to be restricted to 16 main species, with a highlight for T. harzianum and T. asperellum . The two main sources of isolates for these studies (~1/3 each) are institutional collections and rhizospheric soils. Therefore, there is yet plenty of opportunity for bioprospection and basic studies, not only to unravel novel Trichoderma isolates/species bearing abiotic stress-relief effects on plants but also to further understand the underpinning mechanisms of this desirable phenotype.

A tendency was found for the studies to focus on model plants with agronomic/economic relevance, most with short reproductive cycles. Moreover, the competitive ability of Trichoderma species that allows rapid rhizospheric establishment and roots colonization likely explains the preference for experimental inoculations based on soil application and seed coating and biopriming; the ease of later field applications for bioproducts developed in this manner adds to this circumstance. With regard to the abiotic stresses studied in the context of plant-Trichoderma interactions, the focus has been essentially on those caused by excess of salt, drought , and heavy metals, which can be considered as coherent with the major environmental issues affecting the security and sustainability of food production worldwide. As a consequence, the parameters assessed are all directly and indirectly related to shoot and root weight and length, as well as major physiological processes, such as photosynthesis, general cellular redox state and oxidative-stress control/response, and protective compounds synthesis. Not unexpectedly, the molecular and genetic mechanisms studied in this regard have been strictly related with those response variables and could be conceptually classified as transcription factors, metabolic/oxidative stress and signaling pathways, and direct stress-protective molecules. Metanalytical approaches are currently underway to advance the dissection of current information on the Trichoderma effects in the improvement of plant growth and development under abiotic stresses. Taking all this information together, and assessing knowledge-integration studies and reviews, it became evident the astonishing complexity of regulatory mechanisms and networks already unveiled in the Trichoderma-plant interaction, as well as the universe yet to be researched in this field.

We reviewed here the state-of-the-art of knowledge on the use of Trichoderma spp. in aiding plants to cope with a variety of stresses caused by climatic and edaphic abiotic factors; despite some trends and gaps observed in the pertinent investigated literature, the great potential of this fungal genus for developing alternative applications of biotechnological interest (agriculture, industry, environment, and health) is clear. Augmentation of salinity and pollution by an array of xenobiotics (Rosegrant et al. 2009; Munns and Gilliham 2015), as well as global warming effects such as high temperatures, alterations in rainfall cycles, and longer droughts (Godfray et al. 2010; Foley et al. 2011), are relevant examples of these environmental impacts. More than 4/5 of global ecosystems functioning and processes that underpin support services for people are already affected by climate change (Ogar et al. 2020), with a significant role for abiotic factors. The current issues on food production and security will require robust and coordinated actions on scientific and political arenas to bring forth environmentally sustainable solutions for the global economy, hugely impacted by the COVID-19’s pandemic. Those solutions depend upon consistent reductions in both our carbon footprint on the planet (Stern 2016) and in the biodiversity losses, which interdependently affect ecosystems and economy (Dasgupta 2008; Trisos et al. 2020). The large spectrum of compounds and bioproducts that can be extracted from and formulated on the basis of species/isolates of the Trichoderma genus can certainly contribute to broaden the strategies and options for agricultural production with environmental sustainability and safety. Considering current unresolved issues related to the bioproduct registration system and the scope of its applicability, e.g. (Berg et al. 2013; Chojnacka 2015), it may be considered advantageous for a biotechnological product to bear multiple simultaneous functions, a possibility that is clearly present in Trichoderma (Vinale et al. 2008; Schuster and Schmoll 2010; Mukherjee et al. 2013; Hidangmayum et al. 2018). The various biological activities of Trichoderma with beneficial effects for their host plants have a high potential for adding economical and sustainability values to existing and yet to be developed bioproducts and derivatives.