The MdERF61-mdm-miR397b-MdLAC7b module regulates apple resistance to Fusarium solani via lignin biosynthesis

Authors: ZHOU, ZHE - Institute Of Animal Science (CAAS); ZHANG, HAIQING - Institute Of Animal Science (CAAS); YAO, JIALONG - Institute Of Animal Science (CAAS); GAO, QIMING - Institute Of Animal Science (CAAS); WANG, YARONG - Institute Of Animal Science (CAAS); LIU, ZHENZHEN - Institute Of Animal Science (CAAS); ZHANG, YARU - Institute Of Animal Science (CAAS); TIAN, YI - Agricultural University Of Hebei; YAN, ZHENLI - Institute Of Animal Science (CAAS); Zhu, Yanmin; ZHANG, HENGTAO - Institute Of Animal Science (CAAS)

Submitted to: Plant Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/30/2024
Publication Date: 10/7/2024
Citation: Zhou, Z., Zhang, H., Yao, J., Gao, Q., Wang, Y., Liu, Z., Zhang, Y., Tian, Y., Yan, Z., Zhu, Y., Zhang, H. 2024. The MdERF61-mdm-miR397b-MdLAC7b module regulates apple resistance to Fusarium solani via lignin biosynthesis. Plant Physiology. https://doi.org/10.1093/plphys/kiae518.
DOI: https://doi.org/10.1093/plphys/kiae518

Interpretive Summary: Apple replant disease (ARD) is one of the major obstacles in establishing a new apple orchard, which threatened the healthy development of the apple industry. However, the genetic control and molecular regulation underlying disease resistance in apple roots against ARD remains unclear. Based on the findings from our recent genomics study, including comparative transcriptomics, small RNA profiling and degradome sequencing of apple root under pathogenic pressure, the current study focused on a previously identified negative regulatory module, i.e., a microRNA (mdm-miR397b) and its direct target MdLAC7b (a lignin-forming laccase encoding gene), in relation to the effectiveness of defense activation in apple root. The results from current study showed that overexpressing mdm-miR397b-MdLAC7b module altered the lignin deposition patterns and jasmonate (JA) signaling in apple roots. Additionally, Y1H library screening identified an ethylene-responsive transcriptional factor MdERF61 which acts as a repressor for mdm-miR397b transcriptional activity through direct binding to two GCC-boxes in mdm-miR397b promoter. In summary, these results suggest that the MdERF61-mdm-miR397b-MdLAC7b module is an essential regulatory mechanism contributing to apple resistance to F. solani (one of the components in ARD pathogen complex). The findings from current study provide a new perspective and targets for engineering resistance traits in apple roots towards soilborne diseases. Development and deployment of resistant cultivars may offer a more durable, environment-friendly and cost-effective disease management strategy.

Technical Abstract: Apple replant disease (ARD) has become a worldwide problem since it threatened the healthy development of the apple industry. However, the genetic mechanism underlying plant disease resistance against ARD remains unclear. In this study, a negative regulatory microRNA, mdm-miR397b, and its direct target MdLAC7b was selected based on our previous small RNA and degradome sequencing results. Overexpressing mdm-miR397b-MdLAC7b module altered the lignin deposition and JA signaling in apple roots. Additionally, Y1H library screening using mdm-miR397b promoter recombinants identified a transcriptional factor MdERF61 which acts as a repressor for mdm-miR397b transcriptional activity by direct binding to two GCC-boxes in mdm-miR397b promoter. In summary, our results suggest that the MdERF61-mdm-miR397b-MdLAC7b module is essential for apple resistance to F. solani and provide a new perspective for engineering plant resistance to soilborne diseases in apple.