Target of rapamycin signaling orchestrates growth-defense trade-offs in plants.

Plant defense to microbial pathogens is often accompanied by significant growth inhibition. How plants merge immune system function with normal growth and development is still poorly understood. Here, we investigated the role of target of rapamycin (TOR), an evolutionary conserved serine/threonine kinase, in the plant defense response. We used rice as a model system and applied a combination of chemical, genetic, genomic and cell-based analyses. We demonstrate that ectopic expression of TOR and Raptor (regulatory-associated protein of mTOR), a protein previously demonstrated to interact with TOR in Arabidopsis, positively regulates growth and development in rice. Transcriptome analysis of rice cells treated with the TOR-specific inhibitor rapamycin revealed that TOR not only dictates transcriptional reprogramming of extensive gene sets involved in central and secondary metabolism, cell cycle and transcription, but also suppresses many defense-related genes. TOR overexpression lines displayed increased susceptibility to both bacterial and fungal pathogens, whereas plants with reduced TOR signaling displayed enhanced resistance. Finally, we found that TOR antagonizes the action of the classic defense hormones salicylic acid and jasmonic acid. Together, these results indicate that TOR acts as a molecular switch for the activation of cell proliferation and plant growth at the expense of cellular immunity.

The DELLA Protein SLR1 Integrates and Amplifies Salicylic Acid- and Jasmonic Acid-Dependent Innate Immunity in Rice.

Gibberellins are a class of tetracyclic plant hormones that are well known to promote plant growth by inducing the degradation of a class of nuclear growth-repressing proteins, called DELLAs. In recent years, GA and DELLAs are also increasingly implicated in plant responses to pathogen attack, although our understanding of the underlying mechanisms is still limited, especially in monocotyledonous crop plants. Aiming to further decipher the molecular underpinnings of GA- and DELLA-modulated plant immunity, we studied the dynamics and impact of GA and DELLA during infection of the model crop rice (Oryza sativa) with four different pathogens exhibiting distinct lifestyles and infection strategies. Opposite to previous findings in Arabidopsis (Arabidopsis thaliana), our findings reveal a prominent role of the DELLA protein Slender Rice1 (SLR1) in the resistance toward (hemi)biotrophic but not necrotrophic rice pathogens. Moreover, contrary to the differential effect of DELLA on the archetypal defense hormones salicylic acid (SA) and jasmonic acid (JA) in Arabidopsis, we demonstrate that the resistance-promoting effect of SLR1 is due at least in part to its ability to boost both SA- and JA-mediated rice defenses. In a reciprocal manner, we found JA and SA treatment to interfere with GA metabolism and stabilize SLR1. Together, these findings favor a model whereby SLR1 acts as a positive regulator of hemibiotroph resistance in rice by integrating and amplifying SA- and JA-dependent defense signaling. Our results highlight the differences in hormone defense networking between rice and Arabidopsis and underscore the importance of GA and DELLA in molding disease outcomes.

The mitochondrial outer membrane AAA ATPase AtOM66 affects cell death and pathogen resistance in Arabidopsis thaliana.

One of the most stress-responsive genes encoding a mitochondrial protein in Arabidopsis (At3g50930) has been annotated as AtBCS1 (cytochrome bc1 synthase 1), but was previously functionally uncharacterised. Here, we show that the protein encoded by At3g50930 is present as a homo-multimeric protein complex on the outer mitochondrial membrane and lacks the BCS1 domain present in yeast and mammalian BCS1 proteins, with the sequence similarity restricted to the AAA ATPase domain. Thus we propose to re-annotate this protein as AtOM66 (Outer Mitochondrial membrane protein of 66 kDa). While transgenic plants with reduced AtOM66 expression appear to be phenotypically normal, AtOM66 over-expression lines have a distinct phenotype, showing strong leaf curling and reduced starch content. Analysis of mitochondrial protein content demonstrated no detectable changes in mitochondrial respiratory complex protein abundance. Consistent with the stress inducible expression pattern, over-expression lines of AtOM66 are more tolerant to drought stress but undergo stress-induced senescence earlier than wild type. Genome-wide expression analysis revealed a constitutive induction of salicylic acid-related (SA) pathogen defence and cell death genes in over-expression lines. Conversely, expression of SA marker gene PR-1 was reduced in atom66 plants, while jasmonic acid response genes PDF1.2 and VSP2 have increased transcript abundance. In agreement with the expression profile, AtOM66 over-expression plants show increased SA content, accelerated cell death rates and are more tolerant to the biotrophic pathogen Pseudomonas syringae, but more susceptible to the necrotrophic fungus Botrytis cinerea. In conclusion, our results demonstrate a role for AtOM66 in cell death and amplifying SA signalling.

Glutamate metabolism in plant disease and defense: friend or foe?

Plant glutamate metabolism (GM) plays a pivotal role in amino acid metabolism and orchestrates crucial metabolic functions, with key roles in plant defense against pathogens. These functions concern three major areas: nitrogen transportation via the glutamine synthetase and glutamine-oxoglutarate aminotransferase cycle, cellular redox regulation, and tricarboxylic acid cycle-dependent energy reprogramming. During interactions with pathogens, the host GM is markedly altered, leading to either a metabolic state, termed "endurance", in which cell viability is maintained, or to an opposite metabolic state, termed "evasion", in which the process of cell death is facilitated. It seems that endurance-natured modulations result in resistance to necrotrophic pathogens and susceptibility to biotrophs, whereas evasion-related reconfigurations lead to resistance to biotrophic pathogens but stimulate the infection by necrotrophs. Pathogens, however, have evolved strategies such as toxin secretion, hemibiotrophy, and selective amino acid utilization to exploit the plant GM to their own benefit. Collectively, alterations in the host GM in response to different pathogenic scenarios appear to function in two opposing ways, either backing the ongoing defense strategy to ultimately shape an efficient resistance response or being exploited by the pathogen to promote and facilitate infection.

Concurrent overactivation of the cytosolic glutamine synthetase and the GABA shunt in the ABA-deficient sitiens mutant of tomato leads to resistance against Botrytis cinerea.

Deficiency of abscisic acid (ABA) in the sitiens mutant of tomato (Solanum lycopersicum) culminates in increased resistance to Botrytis cinerea through a rapid epidermal hypersensitive response (HR) and associated phenylpropanoid pathway-derived cell wall fortifications. This study focused on understanding the role of primary carbon : nitrogen (C : N) metabolism in the resistance response of sitiens to B. cinerea. How alterations in C : N metabolism are linked with the HR-mediated epidermal arrest of the pathogen has been also investigated. Temporal alterations in the γ-aminobutyric acid (GABA) shunt, glutamine synthetase/glutamate synthase (GS/GOGAT) cycle and phenylpropanoid pathway were transcriptionally, enzymatically and metabolically monitored in both wild-type and sitiens plants. Virus-induced gene silencing, microscopic analyses and pharmacological assays were used to further confirm the data. Our results on the sitiens-B. cinerea interaction favor a model in which cell viability in the cells surrounding the invaded tissue is maintained by a constant replenishment of the tricarboxylic acid (TCA) cycle through overactivation of the GS/GOGAT cycle and the GABA shunt, resulting in resistance through both tightly controlling the defense-associated HR and slowing down the pathogen-induced senescence. Collectively, this study shows that maintaining cell viability via alterations in host C : N metabolism plays a vital role in the resistance response against necrotrophic pathogens.

Spermine Differentially Refines Plant Defense Responses Against Biotic and Abiotic Stresses.

Roles of the major polyamines (mPA), putrescine, spermidine, and spermine (Spm), in various developmental and physiological processes in plants have been well documented. Recently, there has been increasing focus on the link between mPA metabolism and defense response during plant-stress interactions. Empirical evidence is available for a unique role of Spm, distinct from the other mPA, in eliciting an effective defense response to (a)biotic stresses. Our understanding of the precise molecular mechanism(s) by which Spm modulates these defense mechanisms is limited. Further analysis of recent studies indicates that plant Spm functions differently during biotic and abiotic interactions in the regulation of oxidative homeostasis and phytohormone signaling. Here, we summarize and integrate current knowledge about Spm-mediated modulation of plant defense responses to (a)biotic stresses, highlighting the importance of Spm as a potent plant defense activator with broad-spectrum protective effects. A model is proposed to explain how Spm refines defense mechanisms to tailor an optimal resistance response.