Fungi beyond limits: The agricultural promise of extremophiles

Abstract

Global climate changes threaten food security, necessitating urgent measures to enhance agricultural productivity and expand it into areas less for agronomy. This challenge is crucial in achieving Sustainable Development Goal 2 (Zero Hunger). Plant growth-promoting microorganisms (PGPM), bacteria and fungi, emerge as a promising solution to mitigate the impact of climate extremes on agriculture. The concept of the plant holobiont, encompassing the plant host and its symbiotic microbiota, underscores the intricate relationships with a diverse microbial community. PGPM, residing in the rhizosphere, phyllosphere, and endosphere, play vital roles in nutrient solubilization, nitrogen fixation, and biocontrol of pathogens. Novel ecological functions, including epigenetic modifications and suppression of virulence genes, extend our understanding of PGPM strategies. The diverse roles of PGPM as biofertilizers, biocontrollers, biomodulators, and more contribute to sustainable agriculture and environmental resilience. Despite fungi's remarkable plant growth-promoting functions, their potential is often overshadowed compared to bacteria. Arbuscular mycorrhizal fungi (AMF) form a mutualistic symbiosis with many terrestrial plants, enhancing plant nutrition, growth, and stress resistance. Other fungi, including filamentous, yeasts, and polymorphic, from endophytic, to saprophytic, offer unique attributes such as ubiquity, morphology, and endurance in harsh environments, positioning them as exceptional plant growth-promoting fungi (PGPF). Crops frequently face abiotic stresses like salinity, drought, high UV doses and extreme temperatures. Some extremotolerant fungi, including strains from genera like Trichoderma, Penicillium, Fusarium, and others, have been studied for their beneficial interactions with plants. Presented examples of their capabilities in alleviating salinity, drought, and other stresses underscore their potential applications in agriculture. In this context, extremotolerant and extremophilic fungi populating extreme natural environments are muchless investigated. They represent both new challenges and opportunities. As the global climate evolves, understanding and harnessing the intricate mechanisms of fungal-plant interactions, especially in extreme environments, is paramount for developing effective and safe plant probiotics and using fungi as biocontrollers against phytopathogens. Thorough assessments, comprehensive methodologies, and a cautious approach are crucial for leveraging the benefits of extremophilic fungi in the changing landscape of global agriculture, ensuring food security in the face of climate challenges.

FIGURE 1

Some impacts of global warming and the threats posed on attaining the Sustainable Development Goals (SDGs). The sections, arranged sequentially from left to right, examine the principal projected future consequences of climate change on the environment, the interplay between plants, soil, and microbes (including anticipated soil properties under extreme conditions in the future), the productivity of agroecosystems, and the society, that could give rise to humanitarian crises in the near future. The SDGs that may be impacted due to the future extreme scenario are situated at the bottom.

FIGURE 2

Diversity of ecological functions displayed by fungi to promote plant growth and development. Plant growth promoting (PGP) traits displayed by fungi can be grouped according to the impact they have on the growth and development of the plant holobiont through nutrient mobilization or hormone stimulation (Biofertilization), the positive modifications they introduce in the soil on which plants grow (Substrate modification), and the adverse effects they have on pathogens, pests, and herbivores that damages or kill their host plants (Biocontrol). We propose the term ‘Bioengineers’ to denote microorganisms that modify the soil's physical and chemical properties. A different group of PGP‐fungi can also alleviate, in their host plants, the detrimental impact of abiotic stress factors such as drought, salinity, heat, and cold, among others. Finally, some fungi – that we tentatively named ‘Biorecruiters’ – can perform their PGP functions very indirectly, i.e., by stimulating or recruiting other microorganisms belonging to the groups mentioned above of PGP‐organisms. The overall positive impacts of PGP‐fungi on their plant hosts result in improved crop yields and quality. We have highlighted in green the PGP functions confirmed to be displayed by extremophilic/extremotolerant fungi (examples of this kind of fungi are presented in Table 1). We used red letters to distinguish ecological functions displayed by fungi not (yet) confirmed as extremotolerant/extremophiles. The function presented in black (‘pathogen‐helper’ antagonism) has not yet been shown to be displayed by PGP‐fungi.

FIGURE 3

Projects in progress related to the use of extremophilic fungi to develop new bioinputs for agriculture. (A) Use of extremophilic and extremotolerant fungi isolated from the Tehuacán Desert in Mexico to formulate biofertilizers for aromatic plants such as basil, rosemary, mint, and tarragon. (B) Use of fungi associated with quinoa plants for the rational design of biofertilizers based on xerophilic and halophilic fungi to induce protection against salinity and promote plant growth. (C) Use of fungal strains isolated from Mexican volcanoes to protect tomato plants when exposed to extreme temperatures. (D) Use of black yeasts for postharvest control of pathogenic fungi that affect fruits such as apples and tomatoes.