Jul 2026· Proceedings of the National Academy of Sciences of the United States of America· Vol 123 29, pp.
e2609022123
· 0 citations· 69 references
Medicine
TL;DR
Findings establish CDK8 as a regulator that integrates jasmonate signaling with sulfur nutritional status to shape the composition of plant immune responses to shape the composition of plant immune responses.
Abstract
Plant immunity draws heavily on carbon-, nitrogen-, and sulfur-based precursors for the deployment of specialized defense compounds. The jasmonate signaling pathway promotes expression of metabolically costly defenses, often at the expense of growth. How plants coordinate growth-defense tradeoffs with changes in nutrient availability remains poorly understood. Here, we identify CYCLIN-DEPENDENT KINASE 8 (CDK8) as a transcriptional regulator that restrains growth and reduces seed yield under conditions of heightened jasmonate signaling in Arabidopsis thaliana and further show that CDK8 shapes immune responses according to sulfur availability. Transcript and metabolite profiling showed that CDK8 amplifies jasmonate-triggered immunity, including robust accumulation of glucosinolates, camalexin, and sulfur-rich defensin peptides under sulfur-replete conditions. Strikingly, sulfur limitation triggered a CDK8-dependent transcriptional switch that suppressed defensins and glucosinolates while coordinately inducing camalexin, a defense metabolite requiring substantially lower sulfur investment. These findings establish CDK8 as a regulator that integrates jasmonate signaling with sulfur nutritional status to shape the composition of plant immune responses.
It is proposed that sulfur metabolism should be viewed as a dynamic resource allocation network rather than a linear assimilation pathway, to help identify regulatory variants that improve sulfur-use efficiency, stress resilience, immunity, and grain quality without compromising yield stability.
F. Rauf, Hakim Zamir, Hussam Ahmad et al.· Molecular Biotechnology· 0 citations
Plant growth-promoting rhizobacteria (PGPR) enhance host fitness through phytohormone modulation, induced systemic resistance, and pathogen suppression, yet whether variation in bacterial metabolic state independently shapes plant transcriptional response pattern remains unresolved. Here, we compare genome-wide transcriptional responses of Nicotiana benthamiana to a characterized PGPR strain (JS) and a UV-induced mutant (MT) harboring mutations including frameshift disruptions affecting nadB and sacX, genes encoding enzymes involved in NAD⁺ biosynthesis and carbon catabolite regulation. MT-treated plants retained the directional framework of JS-induced transcriptional responses but exhibited attenuated amplitude and redistributed relative transcriptional contribution, consistent with preservation of transcriptional response directionality accompanied by reduced expression amplitude rather than qualitative regulatory replacement. JS exposure coordinated pathways associated with energy metabolism, terpenoid and phenylpropanoid biosynthesis, and plant-pathogen interaction, whereas MT redistributed metabolic emphasis toward carbon and lipid metabolism categories. Hormone-associated analyses revealed that JS promoted coordinated auxin-, gibberellin-, and jasmonate/ethylene-centered signaling, while MT exhibited differential salicylic acid- versus jasmonate-associated weighting, suggesting that bacterial metabolic configuration may contribute to variation in growth-defense hormonal balance. Transcription factor profiling identified reconfigured AP2/ERF, GRAS, Dof, and MADS-box family representation under MT, suggesting that metabolic perturbation is associated with altered representation of upstream regulatory components. Phenotypically, MT reduced shoot growth promotion while preserving root architecture and antifungal efficacy, revealing a functional decoupling between metabolically tunable growth-promoting outputs and resilient biocontrol traits. These findings suggest that metabolically altered bacterial states may be associated with quantitative differences in plant growth- and defense-associated transcriptional responses without altering their directional polarity, and support incorporating bacterial metabolic profiling alongside strain identity as a rational selection criterion for next-generation bioinoculant development in sustainable agriculture.
Seung-A. Kim, Jihyun F. Kim, Soohyun Oh et al.· Plant growth regulation (Pri...· 0 citations
Nonhost resistance (NHR) provides durable and broad-spectrum protection against non-adapted pathogens, yet its regulatory mechanisms in crops remain poorly understood. Here, we show that salicylic acid (SA) signaling plays a critical role in potato NHR against the oomycete pathogen Phytophthora capsici. SA-deficient NahG transgenic plants developed spreading water-soaked lesions following inoculation, whereas wild-type plants exhibited only localized necrosis. Exogenous SA treatment partially restored resistance in NahG lines, supporting an important role for SA in potato NHR. Transcriptome analysis revealed that SA deficiency suppressed defense-associated pathways, including MAPK signaling and pathogenesis-related (PR) gene expression, while inducing photosynthesis- and carbohydrate metabolism-associated genes. In addition, transcriptomic data suggested altered hormone-associated signaling, including induction of ABA-, IAA-, and JA-related pathways, indicating broad transcriptional changes in response to SA deficiency. Functional assays further demonstrated that silencing ERF1B enhanced susceptibility, whereas silencing WRKY53 increased resistance, suggesting distinct transcriptional regulatory roles downstream of SA signaling. Together, these findings support a central role for SA in coordinating immune signaling and metabolic responses during potato nonhost resistance. This study provides new insights into the regulatory framework underlying potato-oomycete interactions.
Phytosulfokine (PSK) is a crucial phytohormone that has been identified for over three decades; however, its transcriptional signaling pathway remains largely unexplored. Here, we disclose a PSK-triggered transcriptional signaling pathway that fine-tunes the tradeoff between growth and immunity in Arabidopsis thaliana. Through forward genetics, we identified the Growth Retardation and Autoimmunity 1 (GRA1) gene, which encodes tyrosylprotein sulfotransferase (TPST), a key enzyme essential for the biosynthesis of sulfated peptides. Notably, similar to the gra1 mutant, the PSK receptor double mutants pskr1 pskr2 also exhibit the gra1-like phenotype, characterized by growth retardation and autoimmunity. Exogenous PSK application rescued the growth defects in gra1 mutants, while overexpression of the PSK precursor gene PSK3 significantly enhanced plant growth. Integrated transcriptomic, genetic, and biochemical analyses demonstrated that PSK represses salicylic acid (SA)-dependent autoimmunity via the transcription factor CAMTA3 to promote plant growth. Mechanistically, PSK attenuates CAMTA3 phosphorylation, thereby enhancing CAMTA3 protein stability and facilitating its nuclear accumulation to constrain SA-mediated autoimmunity. CaM6 and CaM7, two calmodulins that interact with the PSK receptor PSKR1, directly bind to and stabilize CAMTA3. Ectopic expression of CAMTA3 triggers autoimmunity in the cam6 cam7 double mutants but enhances plant growth in wild-type plants, demonstrating that CaM6/7 are indispensable for CAMTA3-dependent growth promotion downstream of PSK signaling. In summary, this study uncovers a previously uncharacterized transcriptional regulatory pathway through which PSK orchestrates the balance between plant growth and immunity.
Penghong Zhang, Yujia Li, F. Yu et al.· Plant Communications· 0 citations
Plants undergo metabolic reprogramming, including senescence, in response to pathogen attack. While senescence-associated genes (SAGs) are critical to this process, the genes that integrate plant defense and senescence processes remain largely unknown. Here, we identified and characterized SENESCENCE ASSOCIATED GENE 1 (SEN1) as a central regulator that coordinates these processes in Arabidopsis. SEN1 is transcriptionally activated by abscisic acid (ABA) via its key component, ABA INSENSITIVE 4 (ABI4). SEN1 interacts with TRXm1, and the interaction modulates sulfotransferase activity of SEN1. Disruption of sen1 and trxm1 mutants reduces reactive oxygen species (ROS), alters the glutathione redox balance (GSH/GSSG), increases susceptibility to pathogens, and delays senescence. Hydrogen sulfide (H2S), a product of SEN1-mediated sulfur transfer, amplifies the module by inducing ABI4 expression. Notably, H2S enhances ABI4 transcriptional activity via persulfuration at Cys250, establishing a self-reinforcing loop. Overall, we propose a regulatory triad in which the ABI4-SEN1-TRXm1 module integrates ABA and H2S signaling to dynamically balance redox homeostasis. This study reveals a molecular switch that fine-tunes plant responses to biotic stress.
Yanke Jiang, K. Fang, Yao Zhang et al.· Plant Communications· 0 citations
Low temperature is a significant abiotic stressor that severely constrains grape cultivation and productivity. Jasmonate ZIM-domain (JAZ) proteins, which function as critical transcriptional repressors in the jasmonic acid signaling pathway, play essential roles in plant stress adaptation. Nevertheless, their specific functions and regulatory mechanisms in grape cold tolerance remain unclear. This work investigated the role and regulatory network of a cold-inducible VvJAZ2 gene by integrating physiological, molecular, and transcriptomic approaches. Functional analyses revealed that overexpression of VvJAZ2 compromised cold tolerance in Arabidopsis and grape calli, manifested as aggravated oxidative damage and compromised antioxidant capacity. Furthermore, transgenic materials exhibited decreased endogenous ABA and JA levels, reduced flavonoid accumulation, and downregulation of the ICE-CBF-COR regulatory module. Consistently, transcriptomic profiling further indicated that VvJAZ2 functions as a negative regulator by coordinating the suppression of ABA/JA signaling cascades, MAPK pathway activity, and flavonoid biosynthetic processes. Mechanistically, the transcription factor VvMSA (Abscisic acid-stress-ripening protein) was identified as an upstream activator that directly binds to the VvJAZ2 promoter and induces its expression under normal conditions; however, this activation is markedly attenuated during cold stress. Moreover, VvJAZ2 physically interacts with VvUGT74F5 (UDP-glycosyltransferase 74F5) implicated in flavonoid modification. Collectively, these findings suggest that VvJAZ2 may function as a potential regulatory node, and support a working model of a dynamic "transcription-protein interaction" module to coordinate hormone signaling and metabolic reprogramming under cold stress. This study provides novel insights into the molecular basis of cold adaptation in grapevine and identifies potential genetic targets for improving cold resilience in viticulture.
Miao Shao, Lili Che, Shixiong Lu et al.· International Journal of Bio...· 0 citations