A holistic overview of the impact of sulfur deficiency in pea facing water deficit

(Virtuel, Présentiel)International audienceWe report on the interplay between water deficit and sulfur deficiency, two constraints that are increasingly faced by crops due to climate change and low-input agricultural practices. In particular, we aim at better understanding the role of sulfur nutrition in the trade-off between seed quality establishment and plant stress tolerance in pea (Pisum sativum L.), a grain legume crop which has a pivotal role to play in both agroecological and food transitions. Like other legumes, pea is able to accumulate large amounts of seed proteins even in the absence of nitrogen fertilizers thanks to its symbiosis with N2-fixing soil bacteria. In this study, we deprived pea plants (cv. Caméor) of sulfur from the mid-vegetative stage and applied a moderate water deficit for 9 days starting at flowering. Individual stresses and control conditions (well-watered, non-limiting sulfur conditions) were applied in parallel for comparison. Phenotypic measurements up to maturity revealed that the combination of the stresses impeded reproductive processes in a synergistic manner, reducing one-seed weight and seed number, thus highlighting the paramount importance of sulfur for maintaining seed yield components when plants encounter a moderate water deficit [1]. Focusing on seed quality attributes, water deficit mitigated the negative effect of sulfur deficiency on the accumulation of sulfur-rich globulins (11S) in mature seeds. Patterns of plant nutrient allocation, including the quantity of sulfur and nitrogen per seed, reflected a lower seed sink strength for nitrogen in the double-stressed plants compared to sulfur-deficient plants. This may readjust the nitrogen to sulfur ratio in the double-stressed seeds, thus rebalancing the amount of 7S (sulfur-poor) and 11S globulins. To uncover the molecular processes underlying the interplay between the two stresses, seeds and leaves, which are respectively sink and source of nutrients, were collected at different time points before, during and after the double stress period and subjected to multi-omics profiling studies. Inference of a protein network using the seed proteomic data identified a cluster of antioxidant proteins (including a glutathione S-transferase, a methionine sulfoxide reductase, and a thioredoxin) that may maintain redox homeostasis in early developing seeds and prevent cellular damage under stress conditions. Integration of these proteomic data with transcriptomic data at the transition to seed filling revealed transcriptional events associated with the accumulation of these antioxidant proteins [2]. This transcriptional defense response mainly involves genes of sulfate homeostasis and assimilation, which is reminiscent to our previous work in Arabidopsis showing that sulfate remobilization in seeds is likely to contribute to the seed's defense against oxidative stress [3]. This study thus provides candidates for targeted studies aimed at dissecting the signaling cascade linking sulfate metabolism to antioxidant processes in developing seeds. These results also highlight the importance of addressing the adaptive mechanisms used by plants to regulate sulfur homeostasis under abiotic constraints. Analysis of the proteomic and transcriptomic data obtained from the leaf samples revealed profound changes in response to water deficit and/or sulfur deficiency, especially when the two stresses were combined. Integration of these data with ionomics data obtained from the same leaf samples, using a weighted-gene co-expression network approach, highlighted genes associated with changes in leaf nutrient concentration, including sulfur concentration. The comparison between leaf transcriptomic and proteomic data allows us to formulate hypotheses on the level of regulation (transcriptional or post-transcriptional) of these genes. We also propose candidate genes that might help plants to better tolerate combinatorial stresses by contributing to adjust nutrient homeostasis in leaves