Integrative multi-omics analysis of rice grown continuously under P-starvation stress unravels Pup1-mediated regulatory complex for resilience to phosphorus deficiency

Phosphorus (P) is a vital macronutrient for various physiological/biochemical activities like ATP production through respiration/photosynthesis, carbohydrate metabolism, nucleic acid/membrane synthesis, intracellular signalling, and functioning of enzymes. To deal with P-starvation/deficiency, plant modulates gene expression for adjusting metabolic/signaling pathways. For P homeostasis, metabolic activities are reoriented by transcriptional as well as post-transcriptional/post-translational modulations to integrate physio-biochemical, (epi)genomic, proteomic, and metabolomic processes. Despite the advances in understanding P-starvation/deficiency responses of plants, the genes/regulatory processes for resilience to low-P stress in plants remain enigmatic. To unravel the genes/pathways and regulatory actions of Pup1 QTL on P-starvation in rice, integrative multi-omics analysis of a near-isogenic line-23 (NIL-23, harboring Pup1 ) and its parental high-yielding rice variety was performed. The multi-omics analysis indicated adoption of multifaceted tolerance mechanisms, integrated nutrient acquisition/transport, hormone signaling, cell wall modification, metabolic modulations, and epigenetic modifications, controlled by Pup1 in NIL-23. Transcriptomic and proteomic analyses highlighted up-regulation of genes/proteins involved in starch/sucrose/nucleotide-sugars metabolism, biosynthesis of secondary metabolites, energy metabolism, and phytohormone signaling in NIL-23. As Pup1 does not carry many protein-coding genes, regulatory functions of the QTL through transcriptomic/epigenetic cascades (via key regulators like transcription factors, chromatin remodelers, and epigenetic factors) modulate gene expression on P-starvation. These affect crucial processes like adaptive changes in plant’s morphology, nutrient acquisition, and metabolic reprogramming in NIL-23. The present study provides a better understanding on Pup1 -mediated regulatory complex for resilience to nutrient/phosphorus deficiency, which might help improving P utilization efficiency of crop plants for enhanced productivity in P-scarce soils. • Phosphorus is crucial for different physio-biochemical processes, including ATP production and functioning of enzyme. • To deal with low-P stress, plants reprogram gene expression to modulate P homeostasis and metabolic pathway. • Regulatory activity of Pup1 QTL on stress was deciphered using a NIL and its parental high-yielding rice variety. • Complementary effect of nutrient acquisition, signaling, epigenetic/metabolic changes play role in stress tolerance. • Reprograming starch/sucrose/energy metabolism, secondary metabolites, cell wall alteration, etc. boosts low-P tolerance.