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Co-option of transcriptional hub expanded triangular functional interactions among nutrients during plant terrestrialzation

ABSTRACT: Plant nitrate, phosphate, and sucrose responses create a complex molecular network fine-tuned for growth and survival. This triangular interplay, crucial for the adaptability of terrestrial plants, allows the availability of one nutrient to influence plant responses to others. However, the origins and functional repurposing of this complex network for plant terrestrialization remain scarcely understood. By delving into the time-series transcriptome responses to nitrate, phosphate, and sucrose in the bryophyte Marchantia polymorpha and its streptophycean algal relatives Klebsormidium nitens, we observed convergent yet largely species-specific regulatory circuits in nutrient response. A key gene regulatory network (GRN) module centered on MpCSD, MpERF20, and MpHD9 was found to govern the hierarchical responses and crosstalk among the three nutrients in M. polymorpha. In K. nitens, these transcription factors were involved in nutrient responses but were co-opted during phytoterrestrialization to serve additional functions. Further network perturbation experiments validated the extensive evolution of transcriptional targets of these regulatory circuits, with cytokinin responsive genes being recruited exclusively into macronutritional GRNs in M. polymorpha thus optimizing nutrient response. Our findings illuminate the evolutionary strategies employed to redeploy the triad of nutrient interactions during the adaptation of ancestral green plants to terrestrial habitats.

ORGANISM(S): Klebsormidium nitens Marchantia polymorpha

PROVIDER: GSE248900 | GEO | 2024/10/16

REPOSITORIES: GEO

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Project description:Transcriptomic analysis in response to Botrytis cinerea infections under conrasting nitrate regime Nitrogen (N) is one of the main limiting nutrients for plant growth and crop yield. It is well documented that changes in nitrate availability, the main N source found in agricultural soils, influences a myriad of developmental programs and processes including the plant defense response. Indeed, many agronomical reports indicate that the plant N nutritional status influences their ability to respond effectively when challenged by different pathogens. However, the molecular mechanisms involved in N-modulation of plant susceptibility to pathogens are poorly characterized. In this work, we show that Solanum lycopersicum defense response to the necrotrophic fungus Botrytis cinerea is affected by plant N availability, with higher susceptibility in nitrate-limiting conditions. Global gene expression responses of tomato against B. cinerea under contrasting nitrate conditions reveals that plant primary metabolism is affected by the fungal infection regardless of N regimes. This result suggests that differential susceptibility to pathogen attack under contrasting N conditions is not only explained by a metabolic alteration. We used a systems biology approach to identify the transcriptional regulatory network implicated in plant response to the fungus infection under contrasting nitrate conditions. Interestingly, hub genes in this network are known key transcription factors involved in ethylene and jasmonic acid signaling. This result positions these hormones as key integrators of nitrate and defense against B. cinerea in tomato plants. Our results provide insights into potential crosstalk mechanisms between necrotrophic defense response and N status in plants. To better understand the molecular changes underlying the impact of nitrate availability on plant susceptibility to B. cinerea, we performed plant transcriptome profiling assays on mock-treated (3 biological replicates) and infected plants ( 3 biological replicates) grown under three N conditions, using GeneChip Tomato Genome Arrays (Affymetrix).

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Co-option of transcriptional hub expanded triangular functional interactions among nutrients during plant terrestrialzation

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