The plant disease triangle facing climate change: a molecular perspective.

Variations in climate conditions can dramatically affect plant health and the generation of climate-resilient crops is imperative to food security. In addition to directly affecting plants, it is predicted that more severe climate conditions will also result in greater biotic stresses. Recent studies have identified climate-sensitive molecular pathways that can result in plants being more susceptible to infection under unfavorable conditions. Here, we review how expected changes in climate will impact plant-pathogen interactions, with a focus on mechanisms regulating plant immunity and microbial virulence strategies. We highlight the complex interactions between abiotic and biotic stresses with the goal of identifying components and/or pathways that are promising targets for genetic engineering to enhance adaptation and strengthen resilience in dynamically changing environments.

Extracellular niche establishment by plant pathogens.

The plant extracellular space, referred to as the apoplast, is inhabited by a variety of microorganisms. Reflecting the crucial nature of this compartment, both plants and microorganisms seek to control, exploit and respond to its composition. Upon sensing the apoplastic environment, pathogens activate virulence programmes, including the delivery of effectors with well-established roles in suppressing plant immunity. We posit that another key and foundational role of effectors is niche establishment - specifically, the manipulation of plant physiological processes to enrich the apoplast in water and nutritive metabolites. Facets of plant immunity counteract niche establishment by restricting water, nutrients and signals for virulence activation. The complex competition to control and, in the case of pathogens, exploit the apoplast provides remarkable insights into the nature of virulence, host susceptibility, host defence and, ultimately, the origin of phytopathogenesis. This novel framework focuses on the ecology of a microbial niche and highlights areas of future research on plant-microorganism interactions.

Evidence of the Involvement of Nematostoma parasiticum in Herpotrichia Needle Browning of Abies balsamea.

Herpotrichia needle browning (HNB) is a disease that affects several species of fir trees in Europe and North America. HNB was first described by Hartig in 1884, who isolated a fungal pathogenic agent identified as responsible for the disease. This fungus was later named Herpotrichia parasitica but is currently named Nematostoma parasiticum. However, the identity of the pathogens causing HNB is regularly questioned and, to date, the true causal agent of this disease has not been definitely established. The present study aimed to identify the fungal populations present in needles of Christmas fir trees (Abies balsamea) and to correlate them with needle health status using robust molecular methods. PCR primers specific to N. parasiticum allowed detection of the presence of this fungus in DNA samples from symptomatic needles. Furthermore, high-throughput sequencing (Illumina MiSeq) clearly showed that N. parasiticum was associated with symptomatic needles. However, high-throughput sequencing results revealed that the presence of other species such as Sydowia polyspora and Rhizoctonia sp. may also correlate with the development of HNB. A diagnostic tool, based on quantitative PCR using a probe, was then developed to detect and quantify N. parasiticum in DNA samples. The efficacy of this molecular approach was validated through the detection of the pathogenic agent in symptomatic needle samples as well as in nonsymptomatic needles collected in trees affected by HNB. In contrast, N. parasiticum could not be found in needles from healthy trees. The present study argues for the importance of N. parasiticum in causing HNB symptoms.

Light prevents pathogen-induced aqueous microenvironments via potentiation of salicylic acid signaling.

Many plant pathogens induce water-soaked lesions in infected tissues. In the case of Pseudomonas syringae (Pst), water-soaking effectors stimulate abscisic acid (ABA) production and signaling, resulting in stomatal closure. This reduces transpiration, increases water accumulation, and induces an apoplastic microenvironment favorable for bacterial growth. Stomata are sensitive to environmental conditions, including light. Here, we show that a period of darkness is required for water-soaking, and that a constant light regime abrogates stomatal closure by Pst. We find that constant light induces resistance to Pst, and that this effect requires salicylic acid (SA). Constant light did not alter effector-induced accumulation of ABA, but induced greater SA production, promoting stomatal opening despite the presence of ABA. Furthermore, application of a SA analog was sufficient to prevent pathogen-induced stomatal closure and water-soaking. Our results suggest potential approaches for interfering with a common virulence strategy, as well as providing a physiological mechanism by which SA functions in defense against pathogens.

A Jasmonic Acid-Related Mechanism Affects ARGONAUTE5 Expression and Antiviral Defense Against Potato Virus X in Arabidopsis thaliana.

During virus infection, Argonaute (AGO) proteins bind to Dicer-produced virus small interfering RNAs and target viral RNA based on sequence complementarity, thereby limiting virus proliferation. The Arabidopsis AGO2 protein is important for resistance to multiple viruses, including potato virus X (PVX). In addition, AGO5 is important in systemic defense against PVX. Normally AGO5 is expressed only in reproductive tissues, and its induction by virus infection is thought to be important for its participation in antiviral defense. However, it is unclear what mechanisms induce AGO5 expression in response to virus infection. Here, we show that dde2-2, a mutant compromised in jasmonic acid (JA) biosynthesis, displays constitutive upregulation of AGO5. This mutant also showed increased resistance to PVX and this resistance was dependent on a functional AGO5 gene. Furthermore, methyl jasmonate treatment ablated AGO5 expression in leaves during virus infection and resulted in increased susceptibility to virus. Our results further support a role for AGO5 in antiviral RNA silencing and a negative regulation by JA, a plant hormone associated with defense against plant-feeding arthropods, which are often the vectors of plant viruses. [Formula: see text] Copyright © 2023 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.

Evolutionarily conserved bacterial effectors hijack abscisic acid signaling to induce an aqueous environment in the apoplast.

High atmospheric humidity levels profoundly impact host-pathogen interactions in plants by enabling the establishment of an aqueous living space that benefits pathogens. The effectors HopM1 and AvrE1 of the bacterial pathogen Pseudomonas syringae have been shown to induce an aqueous apoplast under such conditions. However, the mechanisms by which this happens remain unknown. Here, we show that HopM1 and AvrE1 work redundantly to establish an aqueous living space by inducing a major reprogramming of the Arabidopsis thaliana transcriptome landscape. These effectors induce a strong abscisic acid (ABA) signature, which promotes stomatal closure, resulting in reduced leaf transpiration and water-soaking lesions. Furthermore, these effectors preferentially increase ABA accumulation in guard cells, which control stomatal aperture. Notably, a guard-cell-specific ABA transporter, ABCG40, is necessary for HopM1 induction of water-soaking lesions. This study provides molecular insights into a chain of events of stomatal manipulation that create an ideal microenvironment to facilitate infection.

ARGONAUTE5 Represses Age-Dependent Induction of Flowering through Physical and Functional Interaction with miR156 in Arabidopsis.

Flowering time is a finely tuned process in plants, in part controlled by the age-regulated microRNA156 (miR156), which functions by suppressing the transcripts of SQUAMOSA-PROMOTER BINDING LIKE (SPL) transcription factors. ARGONAUTE (AGO) proteins are essential effectors of miRNA-mediated gene regulation. However, which AGO(s) mediate(s) the control of flowering time remains unclear. Here, we demonstrate a role of AGO5 in controlling flowering time by modulating the expression of SPL transcription factors. We show that AGO5 interacts physically and functionally with miR156 and that ago5 mutants present an early flowering phenotype in Arabidopsis. Furthermore, in ago5 mutants, the repression of flowering caused by miR156 overexpression is largely reversed, whereas leaf morphology remains unaffected. Our results thus indicate a specific role for AGO5 in mediating miR156 activity in meristematic, but not vegetative, tissue. As such, our data suggest a spatiotemporal regulation of the miR156 aging pathway mediated through different AGO proteins in different tissues.

Natural variation in the Arabidopsis AGO2 gene is associated with susceptibility to potato virus X.

RNA silencing functions as an anti-viral defence in plants through the action of DICER-like (DCL) and ARGONAUTE (AGO) proteins. Despite the importance of this mechanism, little is known about the functional consequences of variation in genes encoding RNA silencing components. The AGO2 protein has been shown to be important for defense against multiple viruses, and we investigated how naturally occurring differences in AGO2 between and within species affects its antiviral activities. We find that the AGO2 protein from Arabidopsis thaliana, but not Nicotiana benthamiana, effectively limits potato virus X (PVX). Consistent with this, we find that the A. thaliana AGO2 gene shows a high incidence of polymorphisms between accessions, with evidence of selective pressure. Using functional analyses, we identify polymorphisms that specifically affect AGO2 antiviral activity, without interfering with other AGO2-associated functions such as anti-bacterial resistance or DNA methylation. Our results suggest that viruses adapt to overcome RNA silencing in their hosts. Furthermore, they indicate that plant-virus interactions have influenced natural variation in RNA-silencing components and that the latter may be a source of genetically encoded virus resistance.