Signals and Machinery for Mycorrhizae and Cereal and Oilseed Interactions towards Improved Tolerance to Environmental Stresses

Abstract

In the quest for sustainable agricultural practices, there arises an urgent need for alternative solutions to mineral fertilizers and pesticides, aiming to diminish the environmental footprint of farming. Arbuscular mycorrhizal fungi (AMF) emerge as a promising avenue, bestowing plants with heightened nutrient absorption capabilities while alleviating plant stress. Cereal and oilseed crops benefit from this association in a number of ways, including improved growth fitness, nutrient uptake, and tolerance to environmental stresses. Understanding the molecular mechanisms shaping the impact of AMF on these crops offers encouraging prospects for a more efficient use of these beneficial microorganisms to mitigate climate change-related stressors on plant functioning and productivity. An increased number of studies highlighted the boosting effect of AMF on grain and oil crops' tolerance to (a)biotic stresses while limited ones investigated the molecular aspects orchestrating the different involved mechanisms. This review gives an extensive overview of the different strategies initiated by mycorrhizal cereal and oilseed plants to manage the deleterious effects of environmental stress. We also discuss the molecular drivers and mechanistic concepts to unveil the molecular machinery triggered by AMF to alleviate the tolerance of these crops to stressors.

Keywords: (a)biotic stresses; cereal crops; molecular drivers; mutualism; mycorrhizal symbiosis; oilseed crops; stress mitigation; tolerance.

Figure 1

Molecular mechanisms behind cereal/oilseed–AMF interaction responses to abiotic stresses. After their perception, abiotic stress signals are transduced in the cytoplasm of the mycorrhizal plant cell where they induce the production of ROS by many organelles such as mitochondrion, chloroplast, and peroxisome [48,49]. The accumulation of ROS triggers the activation of various transcription factors that regulate the expression of abiotic stress-responsive genes, thereby stimulating many functioning pathways including stomatal regulation, aquaporin biosynthesis, antioxidant defense system, hormone signaling, and osmoprotectant molecules, leading the improved plant tolerance to abiotic stress [122]. ABA: abscissic acid; ADC: arginine decarboxylase; ERF: ethylene-responsive factors; HMA: heavy metal ATPase; HKT: high-affinity K⁺ transporter; IAA: indole-3-acetic acid; IPS: D-myo-inositol-3-phosphate synthase; 14-3GF: 14-3-3-like protein GF14; MAPK: mitogen-activated protein kinase; NIP: nodulin 26-like intrinsic protein; NRAMP: natural resistance-associated macrophage protein; P5CS: pyrroline-5-carboxylate synthetas; PHT: phosphate transporter; PIP: plasma membrane intrinsic protein; SOS: overly sensitive; TIP: tonoplast intrinsic protein; ZIP: zrt/irt-like protein.

Figure 2

Molecular mechanisms of cereal/oilseed–arbuscular mycorrhizal fungi (AMF) responses to biotic stresses. The diagram depicts the intricate molecular mechanisms involved in the response of cereals/oilseeds to biotic stresses mediated by AMF. Reactive oxygen species (ROS) and Ca²⁺ act as crucial transducers, while mitogen-activated protein kinase (MAPK) cascades play a central role in the crosstalk between Ca²⁺ and ROS, contributing to signal production following exposure to biotic stress [94,149]. Pathogenic microorganisms and plant defense activators, including AMF, bear microbe-associated molecular patterns (MAMPs) on their surface, along with effector proteins that are secreted externally or internally to plant cells. Recognition of MAMPs and effector molecules by pattern recognition receptors (PRRs) leads to the activation of MAMP-triggered immunity (MTI) or effector-triggered immunity (ETI), respectively [150,151]. The activation of defense responses can result in a hypersensitive response (HR), characterized by rapid, localized necrosis at the pathogen’s point of entry. Salicylic acid (SA) and jasmonate/ethylene (JA/ET) orchestrate the plant’s response to biotic stress, with hormones, secondary metabolites, priming agents, and other cytoplasmic chemicals ultimately up-regulating transcription factors (TFs), pathogenesis-related genes (PRs), heat shock protein (HSP) genes, and other defense-related genes [152]. These molecular events collectively contribute to the plant’s protection against biotic stresses.