The Fiber Cell-Specific Overexpression of <i>COMT2</i> Modulates Secondary Cell Wall Biosynthesis in Poplar

Wood, as a natural and renewable resource, plays a crucial role in industrial production and daily life. Lignin, as one of the three major components of the plant cell secondary wall, plays a key role in conferring mechanical strength and enhancing stress resistance. The caffeic acid-O-methyltransferase (COMT) family of oxygen-methyltransferases is a core regulatory node in the downstream pathway of lignin biosynthesis. Here, our report shows that <i>caffeic acid-O-methyltransferase 2</i> (<i>COMT2</i>) exhibits high conservation across several species. Tissue expression analysis reveals that <i>COMT2</i> is specifically highly expressed in the secondary xylem of <i>Populus tomentosa</i> stems. We demonstrated that the specific overexpression of <i>COMT2</i> in fiber cells of <i>Populus tomentosa</i> led to a significant increase in plant height, stem diameter, internode number, and stem dry weight. Furthermore, we found that the specific overexpression of <i>COMT2</i> in fiber cells promotes xylem differentiation, lignin accumulation, and the thickening of the secondary cell wall (SCW) in fiber cells. Our results indicate that key downstream lignin biosynthesis enzyme genes are upregulated in transgenic plants. Additionally, mechanical properties of stem bending resistance, puncture resistance, and compressive strength in the transgenic lines are significantly improved. Moreover, we further created the <i>DUF</i>pro:<i>COMT2</i> transgenic lines of <i>Populus deltoides</i> × <i>Populus. euramericana</i> cv ‘Nanlin895’ to verify the functional conservation of <i>COMT2</i> in closely related poplar species. The <i>DUF</i>pro:<i>COMT2 Populus deltoides</i> × <i>Populus. euramericana</i> cv ‘Nanlin895’ transgenic lines exhibited phenotypes similar to those observed in the <i>P. tomentosa</i> transgenic plants, which showed enhanced growth, increased lignin accumulation, and greater wood strength. Overall, the specific overexpression of the caffeic acid O-methyltransferase gene <i>COMT2</i> in poplar stem fiber cells has enhanced the wood biomass, wood properties, and mechanical strength of poplar stems.