Phosphorus (P) acts as one of the essential macronutrients and plays critical roles in regulating growth, development, and yield formation capacity of the crop plants. Elucidating the physiological and molecular processes underlying plant P deprivation responses benefit the crop cultivation with high P use efficiency (PUE). In this study, we investigated the P-associated and agronomic traits as well as the transcriptome profile under contrasting inorganic phosphorus (Pi) levels combined with deficit irrigation, using two wheat cultivars contrasted by PUE (i.e., high PUE Shixin 828 and P deprivation sensitive Jimai 518). The deficient-P (DP) treatment decreased P accumulative amounts, photosynthetic function, and biomass in plants at various growth stages and reduced yields with respect to sufficient-P (SP) condition. Although the two cultivars were comparable on growth and P-associated traits as well as yields under SP, Shixin 828 displayed better growth traits, more P accumulation, and higher yields than Jimai 518 under DP, suggesting that the high PUE cultivars with enhanced P uptake positively affects photosynthetic function, biomass production, and productivity of plants under P deprivation conditions. A large quantity of genes with differential expression patterns, including 2948 upregulated and 1844 downregulated, were identified based on RNA-seq analysis in the Shixin 828 plants treated with P deprivation. These DE genes were shown to be associated with biological process (i.e., metabolic process and cellular process etc.), cellular components (cell body and organelle etc.), and molecular function (binding and catalytic activity), and phytohormone signaling pathways. Transgene analysis on TaZFP1, a gene in ZFP transcription factor family that exhibited upregulated expression in P-deprived plants, validated its role in enhancing P accumulation and P starvation adaptation of plants. Our results suggested that plant P deprivation response is underlying modulation of various physiological processes via modifying gene transcription at global level.
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