Microbial communities play a pivotal role in the functioning of plants by influencing their physiology and development. While many members of the rhizosphere microbiome are beneficial to plant growth, also plant pathogenic microorganisms colonize the rhizosphere striving to break through the protective microbial shield and to overcome the innate plant defense mechanisms in order to cause disease. A third group of microorganisms that can be found in the rhizosphere are the true and opportunistic human pathogenic bacteria, which can be carried on or in plant tissue and may cause disease when introduced into debilitated humans. Although the importance of the rhizosphere microbiome for plant growth has been widely recognized, for the vast majority of rhizosphere microorganisms no knowledge exists. To enhance plant growth and health, it is essential to know which microorganism is present in the rhizosphere microbiome and what they are doing. Here, we review the main functions of rhizosphere microorganisms and how they impact on health and disease. We discuss the mechanisms involved in the multitrophic interactions and chemical dialogues that occur in the rhizosphere. Finally, we highlight several strategies to redirect or reshape the rhizosphere microbiome in favor of microorganisms that are beneficial to plant growth and health.

The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms

Plants must effectively defend against biotic and abiotic stresses to survive in nature. However, this defense is costly and is often accompanied by significant growth inhibition. How plants coordinate the fluctuating growth-defense dynamics is not well understood and remains a fundamental question. Jasmonate (JA) and gibberellic acid (GA) are important plant hormones that mediate defense and growth, respectively. Binding of bioactive JA or GA ligands to cognate receptors leads to proteasome-dependent degradation of specific transcriptional repressors (the JAZ or DELLA family of proteins), which, at the resting state, represses cognate transcription factors involved in defense (e.g., MYCs) or growth [e.g. phytochrome interacting factors (PIFs)]. In this study, we found that the coi1 JA receptor mutants of rice (a domesticated monocot crop) and Arabidopsis (a model dicot plant) both exhibit hallmark phenotypes of GA-hypersensitive mutants. JA delays GA-mediated DELLA protein degradation, and the della mutant is less sensitive to JA for growth inhibition. Overexpression of a selected group of JAZ repressors in Arabidopsis plants partially phenocopies GA-associated phenotypes of the coi1 mutant, and JAZ9 inhibits RGA (a DELLA protein) interaction with transcription factor PIF3. Importantly, the pif quadruple (pifq) mutant no longer responds to JA-induced growth inhibition, and overexpression of PIF3 could partially overcome JA-induced growth inhibition. Thus, a molecular cascade involving the COI1–JAZ–DELLA–PIF signaling module, by which angiosperm plants prioritize JA-mediated defense over growth, has been elucidated.

/pdf/plant-hormone-jasmonate-prioritizes-defense-over-growth-by-5gtyqm0rj4.pdf

Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade

A biostimulant is an organic material that, when applied in small quantities, enhances plant growth and development such that the response cannot be attributed to the application of traditional plant nutrients. This review is aimed at highlighting developments in the processing of macroalgae for agricultural biostimulants (AB), summarising the biologically active components of brown macroalgae and examining the factors supporting the use of macroalgal AB for managing abiotic and biotic stresses in crop plants. The policy drivers supporting the use of macroalgal-derived ABs in agriculture are also emphasised. We examine the use of macroalgal ABs in crop production and evaluated the benefits of seed priming, foliar application, soil drenches and hydroponic treatments. The use of macroalgal ABs on crop plants can generate multiple benefits with reported effects including enhanced rooting, higher crop and fruit yields, freezing, drought and salt tolerance, enhanced photosynthetic activity and resistance to fungi, bacteria and virus. ABs can be applied as an alternative, or used in conjunction with synthetic crop protection products and plant growth regulators, and may have a role in maintaining crop production levels, health and quality in the future when many active ingredients will be lost to the industry due to changes in European Union regulations. Worldwide, macroalgae remain largely unexploited, we highlight some of the future research and development priorities.

Plant biostimulants: a review on the processing of macroalgae and use of extracts for crop management to reduce abiotic and biotic stresses

The constant struggle between plants and microbes has driven the evolution of multiple defense strategies in the host as well as offense strategies in the pathogen. To defend themselves from pathogen attack, plants often rely on elaborate signaling networks regulated by phytohormones. In turn, pathogens have adopted innovative strategies to manipulate phytohormone-regulated defenses. Tactics frequently employed by plant pathogens involve hijacking, evading, or disrupting hormone signaling pathways and/or crosstalk. As reviewed here, this is achieved mechanistically via pathogen-derived molecules known as effectors, which target phytohormone receptors, transcriptional activators and repressors, and other components of phytohormone signaling in the host plant. Herbivores and sap-sucking insects employ obligate pathogens such as viruses, phytoplasma, or symbiotic bacteria to intervene with phytohormone-regulated defenses. Overall, an improved understanding of phytohormone intervention strategies employed by pests and pathogens during their interactions with plants will ultimately lead to the development of new crop protection strategies.

Intervention of Phytohormone Pathways by Pathogen Effectors

Action of jasmonates in plant stress responses and development--applied aspects.

Complex defense signaling pathways, controlled by different hormones, are involved in the reaction of plants to a wide range of biotic and abiotic stress factors. We studied the ability of salicylic acid, jasmonate (JA), and ethylene (ET) to induce systemic defense in rice (Oryza sativa) against the root knot nematode Meloidogyne graminicola. Exogenous ET (ethephon) and JA (methyl jasmonate) supply on the shoots induced a strong systemic defense response in the roots, exemplified by a major up-regulation of pathogenesis-related genes OsPR1a and OsPR1b, while the salicylic acid analog BTH (benzo-1,2,3-thiadiazole-7-carbothioic acid S-methyl ester) was a less potent systemic defense inducer from shoot to root. Experiments with JA biosynthesis mutants and ET-insensitive transgenics showed that ET-induced defense requires an intact JA pathway, while JA-induced defense was still functional when ET signaling was impaired. Pharmacological inhibition of JA and ET biosynthesis confirmed that JA biosynthesis is needed for ET-induced systemic defense, and quantitative real-time reverse transcription-polymerase chain reaction data revealed that ET application onto the shoots strongly activates JA biosynthesis and signaling genes in the roots. All data provided in this study point to the JA pathway to play a pivotal role in rice defense against root knot nematodes. The expression of defense-related genes was monitored in root galls caused by M. graminicola. Different analyzed defense genes were attenuated in root galls caused by the nematode at early time points after infection. However, when the exogenous defense inducers ethephon and methyl jasmonate were supplied to the plant, the nematode was less effective in counteracting root defense pathways, hence making the plant more resistant to nematode infection.

http://www.plantphysiol.org/content/plantphysiol/157/1/305.full.pdf

The Jasmonate Pathway Is a Key Player in Systemically Induced Defense against Root Knot Nematodes in Rice

The importance of phytohormone balance is increasingly recognized as central to the outcome of plant pathogen interactions. Next to their well-known developmental role, brassinosteroids (BR) were recently found to be involved in plant innate immunity. In this study, we examined the role of BR in rice (Oryza sativa) innate immunity during infection with the root-knot nematode Meloidogyne graminicola, and we studied the inter-relationship with the jasmonate (JA) pathway. Exogenous epibrassinolide (BL) supply at low concentrations induced susceptibility in the roots whereas high concentrations of BL enforced systemic defense against this nematode. Upon high exogenous BL supply on the shoot, quantitative reverse-transcription polymerase chain reaction (qRT-PCR) confirmed a strong feedback inhibitory effect, leading to reduced BR biosynthesis in the root. Moreover, we demonstrate that the immune suppressive effect of BR is at least partly due to negative cross-talk with the JA pathway. Mutants in the BR biosynthesis or signaling pathway accumulate slightly higher levels of the immediate JA-precursor 12-oxo-phytodienoic acid, and qRT-PCR data showed that the BR and JA pathway are mutually antagonistic in rice roots. Collectively, these results suggest that the balance between the BR and JA pathway is an effective regulator of the outcome of the rice M. graminicola interaction.

https://apsjournals.apsnet.org/doi/pdf/10.1094/MPMI-05-12-0108-FI

Brassinosteroids suppress rice defense against root-knot nematodes through antagonism with the jasmonate pathway

One of the reasons for the progressive yield decline observed in aerobic rice production is the rapid build-up of populations of the rice root knot nematode Meloidogyne graminicola. These nematodes induce specialized feeding cells inside root tissue, called giant cells. By injecting effectors in and sipping metabolites out of these cells, they reprogramme normal cell development and deprive the plant of its nutrients. In this research we have studied the transcriptome of giant cells in rice, after isolation of these cells by laser-capture microdissection. The expression profiles revealed a general induction of primary metabolism inside the giant cells. Although the roots were shielded from light induction, we detected a remarkable induction of genes involved in chloroplast biogenesis and tetrapyrrole synthesis. The presence of chloroplast-like structures inside these dark-grown cells was confirmed by confocal microscopy. On the other hand, genes involved in secondary metabolism and more specifically, the majority of defence-related genes were strongly suppressed in the giant cells. In addition, significant induction of transcripts involved in epigenetic processes was detected inside these cells 7 days after infection.

https://biblio.ugent.be/publication/4124100/file/5660292.pdf

Transcriptional analysis through RNA sequencing of giant cells induced by Meloidogyne graminicola in rice roots

Studies involving plant-nematode interactions provide an opportunity to unravel plant defense signaling in root tissues. In this study, we have characterized the roles of salicylate (SA), jasmonate (JA), ethylene (ET) and abscisic acid (ABA) in plant defense against the migratory nematode Hirschmanniella oryzae in the monocot model plant rice (Oryza sativa). Experiments with exogenous hormone applications, biosynthesis inhibition and mutant/transgenic lines were executed to test the effect on H. oryzae parasitism in rice roots. Our results demonstrate that an intact ET, JA and SA biosynthesis pathway is a prerequisite for defense against H. oryzae. By contrast, exogenous ABA treatment drastically compromised the rice defense towards this nematode. Gene expression analyses using quantitative reverse transcription polymerase chain reaction (qRT-PCR) demonstrate that the disease-inducing effect of ABA is likely to be the result of an antagonistic interaction between this hormone and the SA/JA/ET-dependent basal defense system. Collectively, in rice defense against H. oryzae, at least three pathways, namely SA, JA and ET, are important, while ABA plays a negative role in defense. Our results suggest that the balance of ABA and SA/JA/ET signaling is an important determinant for the outcome of the rice-H. oryzae interaction.

https://nph.onlinelibrary.wiley.com/doi/pdf/10.1111/j.1469-8137.2012.04310.x

Abscisic acid interacts antagonistically with classical defense pathways in rice–migratory nematode interaction

Complex defence signalling pathways, controlled by different hormones, are known to be involved in the reaction of plants to a wide range of biotic and abiotic stress factors. Here, we studied the differential expression of genes involved in stress and defence responses in systemic tissue of rice infected with the root knot nematode (RKN) Meloidogyne graminicola and the migratory root rot nematode Hirschmanniella oryzae, two agronomically important rice pathogens with very different lifestyles. qRT-PCR revealed that all investigated systemic tissues had significantly lower expression of isochorismate synthase, a key enzyme for salicylic acid production involved in basal defence and systemic acquired resistance. The systemic defence response upon migratory nematode infection was remarkably similar to fungal rice blast infection. Almost all investigated defence-related genes were up-regulated in rice shoots 3 days after root rot nematode attack, including the phenylpropanoid pathway, ethylene pathway and PR genes, but many of which were suppressed at 7 dpi. Systemic shoot tissue of RKN-infected plants showed similar attenuation of expression of almost all studied genes already at 3 dpi, with clear attenuation of the ethylene pathway and methyl jasmonate biosynthesis. These results provide an interesting starting point for further studies to elucidate how nematodes are able to suppress systemic plant defence mechanisms and the effect in multitrophic interactions.

Kamrun Nahar

Papers

The Jasmonate Pathway Is a Key Player in Systemically Induced Defense against Root Knot Nematodes in Rice

Brassinosteroids suppress rice defense against root-knot nematodes through antagonism with the jasmonate pathway

Transcriptional analysis through RNA sequencing of giant cells induced by Meloidogyne graminicola in rice roots

Abscisic acid interacts antagonistically with classical defense pathways in rice–migratory nematode interaction

Comparing systemic defence-related gene expression changes upon migratory and sedentary nematode attack in rice.