Integrated multi-omics analysis reveals the molecular mechanism underlying poplar 107 rootstock-mediated regulation of Populus tomentosa scion growth.

Abstract

Grafting is widely used for asexual propagation and enhancing plant productivity; however, the molecular mechanisms underlying rootstock-scion interactions remain largely unclear. In this study, Populus × euramericana cv. 'Neva' (poplar 107) served as rootstock and Populus tomentosa 'Yixian' (P. tomentosa) as scion for grafting. By integrating physiological measurements, transcriptome sequencing [messenger RNA (mRNA) and long non-coding RNA (lncRNA)], widely targeted metabolomics, and mobile RNA identification revealed that heterografted scions had increased metabolites related to carbon fixation and metabolism, decreased metabolites associated with respiration and defense, and enhanced net photosynthetic rate, potentially promoting height growth; differential expression lncRNAs may represent an important molecular basis for accelerated scion growth; in scions, mobile mRNA-associated differential mRNAs primarily involved amino acid biosynthesis, while mobile lncRNA-associated ones focused on energy metabolism; no target mRNAs of mobile lncRNAs were found in the rootstock; both mRNAs and lncRNAs were transported in full-length and fragmented forms, and downward RNA transport showed a significant correlation with transcript abundance; in recipient tissues, mobile mRNAs were less abundant while mobile lncRNAs were more abundant than in donor tissues; the flavonoid biosynthesis pathway associated with mobile RNAs played an important role in rootstock-mediated scion growth, and kaempferol, as a key metabolite, reduced reactive oxygen species-induced damage, increased net photosynthetic rate, and promoted growth in Nicotiana benthamiana. This study provides an initial insight into the transport and regulatory patterns of mRNAs and lncRNAs in woody grafted plants, offering a theoretical basis for the rational application of grafting technology.