Invertase PtrNINV1 and sucrose synthase PtrSUS1/2 positively regulate wood development by enhancing carbon supply in Populus trichocarpa

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Sucrose, the main carbon source for plant growth, is hydrolyzed by invertases (INVs) and sucrose synthases (SUSs), which are critical for carbon allocation and sink strength. However, their specific roles in xylem development in Populus remain unclear. Here, knockout mutants of PtrNINV1 and PtrSUS1/2 ( PtrSUS1 and PtrSUS2 ) were generated, and their roles in secondary xylem development were assessed through anatomical observations, wood composition analysis, physiological and biochemical assays, and transcriptomic profiling. Knockout of PtrNINV1 led to a 2.80–3.38 % reduction in cellulose, a 2.06–2.27 % decrease in lignin, and a 1.50–1.54 % increase in hemicellulose, accompanied by a reduction in xylem width, fewer cell layers, and thinner fiber cell walls. Knockout of PtrSUS1/2 induced similar xylem defects as those observed in PtrNINV1 knockout. However, lignin content increased (3.51–4.08 %), while cellulose and hemicellulose decreased (1.92–2.27 % and 0.96–1.13 %, respectively), suggesting a distinct carbon partitioning mechanism for PtrSUS1/2 compared to PtrNINV1. Additionally, PtrNINV1 overexpression in developing xylem enhanced tissue development, highlighting its pivotal role in wood formation. Transcriptomic analysis revealed that PtrNINV1 and PtrSUS1/2 regulate cellulose, hemicellulose, and lignin biosynthesis differently. PtrMYB10 (xylem development key factor) was a ‘hub’ transcription factor in the key carbon metabolism modules of transgenic plants, which also demonstrated the key roles of PtrNINV1 and PtrSUS1/2 in xylem development. This study reveals the synergistic and differential roles of NINVs and SUSs in structural carbon synthesis, which offer a strategy for precise control of wood composition.

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