Dehydration-induced alterations in chloroplast proteome and reprogramming of cellular metabolism in developing chickpea delineate interrelated adaptive responses

Abstract

Chloroplast, the energy organelle unique to photosynthetic eukaryotes, executes several crucial functions including photosynthesis. While chloroplast development and function are controlled by the nucleus, environmental stress modulated alterations perceived by the chloroplasts are communicated to the nucleus via retrograde signaling. Notably, coordination of chloroplast and nuclear gene expression is synchronized by anterograde and retrograde signaling. The chloroplast proteome holds significance for stress responses and adaptation. We unraveled dehydration-induced alterations in the chloroplast proteome of a grain legume, chickpea and identified an array of dehydration-responsive proteins (DRPs) primarily involved in photosynthesis, carbohydrate metabolism and stress response. Notably, 12 DRPs were encoded by chloroplast genome, while the rest were nuclear-encoded. We observed a coordinated expression of different multi-subunit protein complexes viz., RuBisCo, photosystem II and cytochrome b6f, encoded by both chloroplast and nuclear genome. Comparison with previously reported stress-responsive chloroplast proteomes showed unique and overlapping components. Transcript abundance of several previously reported markers of retrograde signaling revealed relay of dehydration-elicited signaling events between chloroplasts and nucleus. Additionally, dehydration-triggered metabolic adjustments demonstrated alterations in carbohydrate and amino acid metabolism. This study offers a panoramic catalogue of dehydration-responsive signatures of chloroplast proteome and associated retrograde signaling events, and cellular metabolic reprograming.