# Grasping Molecular Biology Mechanisms to Optimize Plant Resistance and Advance Microbiome Role Against Phytonematodes

## TL;DR

This review explores how plant microbiomes and molecular strategies can enhance plant resistance to parasitic nematodes and improve crop management.

## Contribution

The paper introduces novel microbiome-based strategies and genetic engineering techniques to optimize plant resistance against phytonematodes.

## Key findings

- CRISPR/Cas9 successfully knocks out genes in rice and cotton to confer nematode resistance without yield loss.
- Microbiome inoculants and systemic acquired resistance (SAR) mediated by salicylic acid can prime plant defenses.
- Advanced molecular tools are needed to distinguish microbiome strains with divergent functional traits.

## Abstract

Plant-parasitic nematodes (PPNs) cause big crop losses globally. Safe/reliable methods for their durable management strategies can harness various beneficial relationships among the plant immune system and related microbiomes. Molecular mechanisms basic to these relations reveal wide arrays of significant roles for plant-healthy growth. This review focuses on such relations of microbiomes to prime and immunize plants against PPNs. It also highlights molecular issues facing PPN-resistant varieties with possible solutions such as genetic breeding/engineering, grafting, PPN-antagonistic root exudates, and novel resistant cultivars. These issues call for optimal uses of various widespread groups of microbiomes. Related plant signaling hormones and transcription factors that regulate gene expression and modulate nematode-responsive genes to ease positive/negative adaptation are presented. Exploring PPN-resistance genes, their activation mechanisms, and signaling networks offers a holistic grasp of plant defense related to biotic/abiotic factors. Such factors relevant to systemic acquired resistance (SAR) via plant–microbe interactions to manage PPNs are stressed. The microbiomes can be added as inoculants and/or steering the indigenous rhizosphere ones. Consequently, SAR is mediated by the accumulation of salicylic acid and the subsequent expression of pathogenesis-related genes. To activate SAR, adequate priming and induction of plant defense against PPNs would rely on closely linked factors. They mainly include the engaged microbiome species/strains, plant genotypes, existing fauna/flora, compatibility with other involved biologicals, and methods/rates of the inoculants. To operationalize improved plant resistance and the microbiome’s usage, novel actionable insights for research and field applications are necessary. Synthesis of adequate screening techniques in plant breeding would better use multiple parameters (molecular and classical ones)-based ratings for PPN-host suitability designation. Sound statistical analyses and interpretation approaches can better identify genotypes with high-level, stable resistance to PPNs than the commonly used ones. Linking molecular mechanisms to consistent field relevance can be progressed via dissemination of many advanced techniques. The CRISPR/Cas9 system has been effective in knocking out both the OsHPP04 gene in rice to confer resistance against Meloidogyne graminicola and the GhiMLO3 gene in cotton to minimize the Rotylenchulus reniformis reproduction. Its genetic modifications in crops synthesized “transgene-free” PPN-resistant plants without decreased growth/yield. Characterizing microbiome species/strains needed to prime and immunize plants requires better molecular tools for fine-scale taxonomic resolution than the common ones used. The former can distinguish closely related ones that exhibit divergent phenotypes for key attributes like stability and production of enzymes and secondary metabolites. As PPN-control strategies via tritrophic interactions are more sensitive to the relevant settings than chemical nematicides, it is suggested herein to test these settings on a case-by-case basis to avoid erratic/contradictory results. Moreover, expanding the use of automated systems to expedite detection/count processes of PPN and related microbes with objectivity/accuracy is discussed. When PPNs and their related microbial distribution patterns were modeled, more aspects of their field distributions were discovered in order to optimize their integrated management. Hence, the feasibility of site-specific microbiome application in PPN–hotspot infections can be evaluated. The main technical challenges and controversies in the field are also addressed herein. Their conceptual revision based on harnessing novel techniques/tools is direly needed for future clear trends. This review also engages raising growers’ awareness to leverage such strategies for enhancing plant resistance and advancing the microbiome role. Microbiomes enjoy wide spectrum efficacy, low fitness cost, and inheritance to next generations in durable agriculture.