Comprehensive transcriptome and metabolome analysis deciphers the mechanism underlying rapid xylem growth in the dominant hybrid poplar QB3.

Abstract

Main conclusion: Compared with its parents, the heterosis in growth of QB3 is primarily attributed to the upregulation of auxin and brassinosteroid-related genes, as well as the induced expression of numerous xylem and phloem synthesis genes, particularly the accumulation of lignin. Interestingly, QB3 significantly increased resistance to gray mold, which may be related to anthocyanin accumulation. Our findings illuminate the complex interplay of biological mechanisms that govern the regulation of wood growth and resistance. Poplar, as a fast-growing energy species widely distributed in the northern hemisphere, has important ecological and economic value. The hybridization of poplars is very common and often can bring to the progeny superior growth and resilience traits, but the molecular mechanism of heterosis remains to be studied. Through decades of crossbreeding work, a high-growth rate hybrid offspring named QinBai3 (QB3) was selected from P. alba × (P. alba × P. glandulosa), which provided an ideal model for investigating the molecular mechanism of heterosis. We found that the plant height, ground diameter, and xylem thickness of QB3 were much higher than those of I101 and 84 K. Through transcriptome and qRT-PCR analyses, we found that the expression levels of poplar regulatory genes associated with vegetative growth, brassinosteroid (BR), and auxin hormone signaling were significantly elevated in July compared to February. Meanwhile, compared to its parents, QB3 exhibited more specifically up-regulated genes in the processes of xylem and phloem synthesis, notably PalOPS and PalPRX52. However, in response to certain abiotic stresses, such as water deprivation and UV-B exposure, more down-regulated genes were identified. Metabolome analyses indicated that QB3 significantly increased the levels of lignin and anthocyanin, a result that aligns with the transcriptome data. Additionally, chemical assays confirmed the substantial accumulation of lignin and anthocyanin in QB3, suggesting that increased lignin accumulation may enhance the stem growth rate of QB3. Surprisingly, QB3 significantly increased resistance to Botrytis cinerea B05.10, which was accompanied by anthocyanin accumulation. In addition, our study offers detailed insights into the molecular mechanisms underlying rapid growth and stress resistance in hybrid poplar, thereby providing a new theoretical foundation and practical guidance for forest genetic breeding.