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

Bin Xie; Yanhui Chen; Yanzhen Zhang; Xiuhong An; Xin Li; An Yang; Guodong Kang; Jiangtao Zhou; Cungang Cheng

doi:10.3389/fpls.2023.1120777

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

Front Plant Sci. 2023 Jun 19:14:1120777. doi: 10.3389/fpls.2023.1120777. eCollection 2023.

Authors

Bin Xie¹, Yanhui Chen¹, Yanzhen Zhang¹, Xiuhong An², Xin Li¹, An Yang¹, Guodong Kang¹, Jiangtao Zhou¹, Cungang Cheng¹

Affiliations

¹ Key Laboratory of Mineral Nutrition and Efficient Fertilization for Deciduous Fruits, Liaoning Province/Key Laboratory of Fruit Germplasm Resources Utilization, Ministry of Agriculture and Rural Affairs/Research Institute of Pomology, Chinese Academy of Agricultural Sciences, Xingcheng, Liaoning, China.
² Research Center for Agricultural Engineering Technology of Mountain District of Hebei/Mountainous Areas Research Institute, Hebei Agricultural University, Baoding, Hebei, China.

Abstract

Nitrogen (N) and phosphorus (P) are essential phytomacronutrients, and deficiencies in these two elements limit growth and yield in apple (Malus domestica 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 ${NO}_{3}^{-}$ 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 MdEXPA4 and MdEXLB1, two cell wall expansin genes, were shown to be induced by N and/or P deficiency. Overexpression of MdEXPA4 enhanced root development and improved tolerance to N and/or P deficiency in transgenic Arabidopsis thaliana plants. In addition, overexpression of MdEXLB1 in transgenic Solanum lycopersicum 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.

Keywords: apple dwarfing rootstock; cell wall; expansin; nitrogen and phosphorus deficiencies; root architecture.

Grants and funding

This research was funded by the National Natural Science Foundation of China (32202413), Agricultural Science and Technology Innovation Program (No. CAAS-ASTIP-2016-RIP-02), earmarked fund for China Agriculture Research System (No. CARS-27), and Natural Science Foundation of Hebei Province (C2021204134).