Abstract
Polyploid plants frequently exhibit altered vegetative growth, yet the molecular mechanisms remain unclear. This study reveals that hexaploidisation of triploid insect-resistant poplar 741-line Pb29 significantly reduces growth rate, leaf area, photosynthetic capacity and organic matter accumulation. Meanwhile, the degradation of auxin and gibberellic acid accelerated, the abscisic acid content increased, and insect resistance was diminished with the increase in ploidy. Comprehensive multiomics analysis elucidated the molecular mechanisms underlying the slow vegetative growth of hexaploids. Transcriptome analysis demonstrated reshaping of vegetative growth-associated networks, manifested as reduced photosynthetic capacity and increased energy consumption, which ultimately reduced the energy available for vegetative growth. Differential expression of miR319, novel-m0126-5p and ptc-miR6427-3p altered the transcription levels of vegetative growth-related genes. The genome of hexaploids exhibited significantly elevated DNA methylation levels, and significant changes in DNA methylation levels in vegetative growth-related specific regions can affect the growth and development of hexaploids. Notably, we identified an ethylene response factor gene, ERF016-like, in the vegetative growth regulatory network, and further experiments demonstrated that ERF016-like negatively regulates plant vegetative growth by altering the accumulation of sugars produced through photosynthesis, the production of ATP, and the response to auxin. In summary, the slow vegetative growth of the hexaploids is a comprehensive manifestation of interactions in multilevel molecular regulatory networks. This phenomenon is related to adjustment of the gene expression network and changes in post-transcriptional miRNA regulation as well as epigenetic modifications. These complex regulatory mechanisms work together to cause the slow vegetative growth and development characteristics of hexaploids.