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Plants have to cope with a myriad of soilborne pathogens that affect crop production and food security. The complex interactions between the root system and microorganisms are determinant for the whole plant health. However, the knowledge regarding root defense responses is limited as compared to the aerial parts of the plant. Immune responses in roots appear to be tissue-specific suggesting a compartmentalization of defense mechanisms in these organs. The root cap releases cells termed root “associated cap-derived cells” (AC-DCs) or “border cells” embedded in a thick mucilage layer forming the root extracellular trap (RET) dedicated to root protection against soilborne pathogens. Pea ( Pisum sativum ) is the plant model used to characterize the composition of the RET and to unravel its function in root defense. The objective of this paper is to review modes of action of the RET from pea against diverse pathogens with a special focus on root rot disease caused by Aphanomyces euteiches , one of the most widely occurring and large-scale pea crop diseases. The RET, at the interface between the soil and the root, is enriched in antimicrobial compounds including defense-related proteins, secondary metabolites, and glycan-containing molecules. More especially arabinogalactan proteins (AGPs), a family of plant extracellular proteoglycans belonging to the hydroxyproline-rich glycoproteins were found to be particularly present in pea border cells and mucilage. Herein, we discuss the role of RET and AGPs in the interaction between roots and microorganisms and future potential developments for pea crop protection.

Background Apple replant disease is a soilborne disease caused by Fusarium proliferatum f. sp. malus domestica strain MR5 (abbreviated hereafter as Fpmd MR5) in China. This pathogen causes root tissue rot and wilting leaves in apple seedlings, leading to plant death. A comparative transcriptome analysis was conducted using the Illumina Novaseq platform to identify the molecular defense mechanisms of the susceptible M.26 and the resistant M9T337 apple rootstocks to Fpmd MR5 infection. Results Approximately 518.1 million high-quality reads were generated using RNA sequencing (RNA-seq). Comparative analysis between the mock-inoculated and Fpmd MR5 infected apple rootstocks revealed 28,196 significantly differentially expressed genes (DEGs), including 14,572 up-regulated and 13,624 down-regulated genes. Among them, the transcriptomes in the roots of the susceptible genotype M.26 were reflected by overrepresented DEGs. MapMan analysis indicated that a large number of DEGs were involved in the response of apple plants to Fpmd MR5 stress. The important functional groups identified via gene ontology (GO) and the Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment were responsible for fundamental biological regulation, secondary metabolism, plant-pathogen recognition, and plant hormone signal transduction (ethylene and jasmonate). Furthermore, the expression of 33 up-regulated candidate genes (12 related to WRKY DNA-binding proteins, one encoding endochitinase, two encoding beta-glucosidases, ten related to pathogenesis-related proteins, and eight encoding ethylene-responsive transcription factors) were validated by quantitative real-time PCR. Conclusion RNA-seq profiling was performed for the first time to analyze response of apple root to Fpmd MR5 infection. We found that the production of antimicrobial compounds and antioxidants enhanced plant resistance to pathogens, and pathogenesis-related protein (PR10 homologs, chitinase, and beta-glucosidase) may play unique roles in the defense response. These results provide new insights into the mechanisms of the apple root response to Fpmd MR5 infection.

Grasses (Poaceae) are the fifth-largest plant family by species and their uses for crops, forage, fiber, and fuel make them the most economically important. In grasslands, which broadly-defined cover 40% of the Earth's terrestrial surface outside of Greenland and Antarctica, 40-60% of net primary productivity and 70-98% of invertebrate biomass occurs belowground, providing extensive scope for interactions between roots and rhizosphere invertebrates. Grasses invest 50-70% of fixed carbon into root construction, which suggests roots are high value tissues that should be defended from herbivores, but we know relatively little about such defenses. In this article, we identify candidate grass root defenses, including physical (tough) and chemical (toxic) resistance traits, together with indirect defenses involving recruitment of root herbivores' natural enemies. We draw on relevant literature to establish whether these defenses are present in grasses, and specifically in grass roots, and which herbivores of grasses are affected by these defenses. Physical defenses could include structural macro-molecules such as lignin, cellulose, suberin, and callose in addition to silica and calcium oxalate. Root hairs and rhizosheaths, a structural adaptation unique to grasses, might also play defensive roles. To date, only lignin and silica have been shown to negatively affect root herbivores. In terms of chemical resistance traits, nitrate, oxalic acid, terpenoids, alkaloids, amino acids, cyanogenic glycosides, benzoxazinoids, phenolics, and proteinase inhibitors have the potential to negatively affect grass root herbivores. Several good examples demonstrate the existence of indirect defenses in grass roots, including maize, which can recruit entomopathogenic nematodes (EPNs) via emission of (E)-β-caryophyllene, and similar defenses are likely to be common. In producing this review, we aimed to equip researchers with candidate root defenses for further research.

Plants experience seasonal fluctuations in abiotic and biotic factors such as herbivore attack rates. If and how root defense expression co-varies with seasonal fluctuations in abiotic factors and root herbivore attack rates is not well understood. Here, we evaluated seasonal changes in defensive root latex chemistry of Taraxacum officinale plants in the field and correlated the changes with seasonal fluctuations in abiotic factors and damage potential by Melolontha melolontha, a major natural enemy of T. officinale. We then explored the causality and consequences of these relationships under controlled conditions. The concentration of the defensive sesquiterpene lactone taraxinic acid β-D glucopyranosyl ester (TA-G) varied substantially over the year and was most strongly correlated to mean monthly temperature. Both temperature and TA-G levels were correlated with annual fluctuations in potential M. melolontha damage. Under controlled conditions, plants grown under high temperature produced more TA-G and were less attractive for M. melolontha. However, temperature-dependent M. melolontha feeding preferences were not significantly altered in TA-G deficient transgenic lines. Our results suggest that fluctuations in temperature leads to variation in the production of a root defensive metabolites that co-varies with expected attack of a major root herbivore. Temperature-dependent herbivore preference, however, is likely to be modulated by other phenotypic alterations.

Herbivore‐induced defences in plants are considered a strategy to manage multiple interactions while saving resources. The optimal defence theory (ODT) is one of the most prominent theoretical frameworks to explain the defence allocation patterns within plants. It was recently shown that the ODT generally applies to constitutive glucosinolate (GSL) allocation in shoot and root organs. Previous studies showed that both root and shoot herbivore feeding may alter defence allocation over plant organs. For shoots, the effect depends on where the herbivores feed. It is as yet unknown whether similar principles apply to root‐herbivore‐induced GSLs. To analyse the effects of root localized herbivore feeding on GSL allocation, we conducted a pot experiment using Anomala cuprea grubs and four Brassicaceae; Brassica rapa, B. nigra, B. oleracea and Sinapis alba. Individuals of these four plant species were grown in dedicated mesocosms. The grubs were confined either to the bottom soil, the middle section or the topsoil. Plants grown in the same set‐ups but without root herbivores served as controls. Glucosinolate levels of the leaf lamina, petiole and stem as well as of the taproot, lateral roots and fine roots were measured after 8 days of herbivory. Plant biomass reduction due to herbivory was the largest when herbivores were confined to the topsoil. In the three Brassica species, taproot GSL levels increased upon herbivory independent of where the root herbivores were feeding. Glucosinolate levels in fine roots and shoots, on the other hand, hardly responded to root herbivory. Indole GSLs, which are more effective to pathogens than to herbivores, were more strongly induced than aliphatic and aromatic GSLs, especially in the taproots. Sinapis alba did not show remarkable increments in any GSL level upon herbivory. These results show that locally and systemically induced defences in roots are consistent with the ODT: The taproot which is the most vulnerable and valuable to plant performance shows the highest increase in defence induction. The induced GSL profiles suggest that the response may not only target herbivores, but may also help to prevent secondary infection by microbial pathogens. A plain language summary is available for this article. Plain Language Summary

Numerous empirical studies have examined ontogenetic trajectories in plant defenses but only a few have explored the potential mechanisms underlying those patterns. Furthermore, most documented ontogenetic trajectories in plant defenses have generally concentrated on aboveground tissues; thus, our knowledge regarding whole plant trends in plant defenses throughout development or potential allocation constraints between growth and defenses is limited. Here, we document changes in plant biomass, nutritional quality and chemical defenses for below-and aboveground tissues across seven age classes of Plantago lanceolata (Plantaginaceae) to evaluate: (1) partial and whole plant ontogenetic trajectories in constitutive chemical defenses and nutritional quality, and (2) the role of resource allocation constraints, namely root: shoot (R: S) ratios, in explaining whole plant investment in chemical defenses over time. Overall investment in iridoid glycosides (IGs) significantly increased, while water and nitrogen concentrations in shoot tissues decreased with plant age. Significant variation in IG content between shoot and root tissues across development was observed: allocation of IGs into root tissues linearly increased from younger to older plants, while non-linear shifts in allocation of IGs during ontogeny were observed for shoot tissues. Finally, R: S ratios only weakly explained overall allocation of resources into defenses, with young stages showing a positive relationship, while older stages showed a negative relationship between R: S ratios and IG concentrations. Ontogenetic trajectories in plant quality and defenses within and among plant tissues can strongly influence insect herbivores' performance and/or prédation risk; thus, they are likely to play a significant role in mediating species interactions.

Mentioned for the first time in an article 1971, the occurrence of the term “ Macrophomina phaseolina ” has experienced a steep increase in the scientific literature over the past 15 years. Concurrently, incidences of M. phaseolina -caused crop diseases have been getting more frequent. The high levels of diversity and plasticity observed for M. phasolina genomes along with a rich equipment of plant cell wall degrading enzymes, secondary metabolites and putative virulence effectors as well as the unusual longevity of microsclerotia, their asexual reproduction structures, make this pathogen very difficult to control and crop protection against it very challenging. During the past years several studies have emerged reporting on host defense measures against M. phaseolina , as well as mechanisms of pathogenicity employed by this fungal pathogen. While most of these studies have been performed in crop systems, such as soybean or sesame, recently interactions of M. phaseolina with the model plant Arabidopsis thaliana have been described. Collectively, results from various studies are hinting at a complex infection cycle of M. phaseolina , which exhibits an early biotrophic phase and switches to necrotrophy at later time points during the infection process. Consequently, responses of the hosts are complex and seem coordinated by multiple defense-associated phytohormones. However, at this point no robust and strong host defense mechanism against M. phaseolina has been described.

Aims Studies have shown that arbuscular mycorrhizal (AM) fungi can reduce the performance of typically detrimental root feeding insects, yet the mechanisms remain unclear. This study aimed to investigate the effects of different sources of AM inocula on plant resistance to a root feeding insect in two different soils with different silicon (Si) concentrations. Methods Sugarcane (Saccharum spp. hybrid) was grown in high or low Si soil; plants were treated with either an inoculum comprising the native AM fungi, a commercial AM fungal inoculum or with no AM fungi. Root herbivore (Dermolepida albohirtum) performance was measured in a feeding assay. Results In the low Si soil AM fungi increased root Si concentrations and reduced root herbivore performance. Both commercial and native AM treatments increased root Si and also reduced root herbivore growth rates by 107% and 81%, respectively. AM colonisation positively correlated with root Si concentrations. Distinct from this, in the high Si soil AM fungi had no impact on root Si or root herbivore growth. However, root consumption was reduced; a response independent of Si concentrations. Conclusions Our study suggests AM fungi can enhance Si based plant defences against root herbivores, but also highlights that interactions between AM fungi and root herbivores involves multiple mechanisms requiring further research.

The implementation of agroecological practices aims at promoting productivity and reducing environmental impacts due to the excessive use of mineral fertilizers and pesticides. It relies on soil microbiota beneficial activities, such as the efficient use of water and natural soil resources and the provision of important ecosystem services. This review will focus on arbuscular mycorrhizal fungi (AMF) and their role in weed management. AMF are soil beneficial microorganisms establishing mutualistic symbiotic associations with the roots of most food crops and playing key roles in plant growth, nutrition and health. Several plant species are unable to form functional mycorrhizal symbioses (nonhost plants), lacking “symbiotic-specific” genes, as shown by genomic, transcriptomic and phylogenomic analyses. The majority of nonhost plants belong to families encompassing some of the world’s worst agricultural weed species, such as Chenopodium album , Raphanus raphanistrum , Rapistrum rugosum , Capsella bursa-pastoris and Sinapis arvensis . The nonhost mycorrhizal status entails adverse effects on nonhost weeds due to attempted fungal colonisation, leading to reduced plant survival, growth and nutrient acquisition, particularly when grown in the presence of active AMF extraradical hyphae originating from host plants. These effects have been attributed to the activation of plant root defenses diverting resources from plant growth. This review provides qualitative and quantitative data on the interactions between AMF and nonhost weeds and on the mechanisms underlying weed fitness reduction. The lack of extensive field studies highlights the need for experimental works under real crop conditions to determine whether the combination of AMF with cover crops – a weed management practice adopted in agroecology – could serve as a valuable strategy for weed control, promoting the agroecological transition towards low-input, safe, and resilient agroecosystems.

Below-ground (BG) symbionts of plants can have substantial influence on plant growth and nutrition. Recent work demonstrates that mycorrhizal fungi can affect plant resistance to herbivory and the performance of above- (AG) and BG herbivores. Although these examples emerge from diverse systems, it is unclear if plant species that express similar defensive traits respond similarly to fungal colonization, but comparative work may inform this question. To examine the effects of arbuscular mycorrhizal fungi (AMF) on the expression of chemical resistance, we inoculated 8 species of Asclepias (milkweed)-which all produce toxic cardenolides-with a community of AMF. We quantified plant biomass, foliar and root cardenolide concentration and composition, and assessed evidence for a growth-defense tradeoff in the presence and absence of AMF. As expected, total foliar and root cardenolide concentration varied among milkweed species. Importantly, the effect of mycorrhizal fungi on total foliar cardenolide concentration also varied among milkweed species, with foliar cardenolides increasing or decreasing, depending on the plant species. We detected a phylogenetic signal to this variation; AMF fungi reduced foliar cardenolide concentrations to a greater extent in the clade including A. curassavica than in the clade including A. syriaca. Moreover, AMF inoculation shifted the composition of cardenolides in AG and BG plant tissues in a species-specific fashion. Mycorrhizal inoculation changed the relative distribution of cardenolides between root and shoot tissue in a species-specific fashion, but did not affect cardenolide diversity or polarity. Finally, a tradeoff between plant growth and defense in non-mycorrhizal plants was mitigated completely by AMF inoculation. Overall, we conclude that the effects of AMF inoculation on the expression of chemical resistance can vary among congeneric plant species, and ameliorate tradeoffs between growth and defense.