Comparative physiological, metabolomic, and transcriptomic analyses reveal mechanisms of apple dwarfing rootstock root morphogenesis under nitrogen and/or phosphorus deficient conditions.

Nitrogen (N) and phosphorus (P) are essential phytomacronutrients, and deficiencies in these two elements limit growth and yield in apple ( Borkh.). The rootstock plays a key role in the nutrient uptake and environmental adaptation of apple. The objective of this study was to investigate the effects of N and/or P deficiency on hydroponically-grown dwarfing rootstock 'M9-T337' seedlings, particularly the roots, by performing an integrated physiological, transcriptomics-, and metabolomics-based analyses. Compared to N and P sufficiency, N and/or P deficiency inhibited aboveground growth, increased the partitioning of total N and total P in roots, enhanced the total number of tips, length, volume, and surface area of roots, and improved the root-to-shoot ratio. P and/or N deficiency inhibited influx into roots, and H pumps played a important role in the response to P and/or N deficiency. Conjoint analysis of differentially expressed genes and differentially accumulated metabolites in roots revealed that N and/or P deficiency altered the biosynthesis of cell wall components such as cellulose, hemicellulose, lignin, and pectin. The expression of and , two cell wall expansin genes, were shown to be induced by N and/or P deficiency. Overexpression of enhanced root development and improved tolerance to N and/or P deficiency in transgenic plants. In addition, overexpression of in transgenic seedlings increased the root surface area and promoted acquisition of N and P, thereby facilitating plant growth and adaptation to N and/or P deficiency. Collectively, these results provided a reference for improving root architecture in dwarfing rootstock and furthering our understanding of integration between N and P signaling pathways.