Evolution of the JULGI-SMXL4/5 module for phloem development in angiosperms

• 成果类型: Article
• 署名作者: Park, Chanyoung; Cho, Hyun Seob; Lim, Yookyung; Cho, Chung Hyun; Nam, Hoyoung; Choi, Sangkyu; Lim, Hojun; Kim, Young - Dong; Yoon, Hwan Su; Cho, Hyunwoo; Hwang, Ildoo
• 署名单位: Pohang University of Science & Technology (POSTECH); Chungbuk National University; Austrian Academy of Sciences; Vienna Biocenter (VBC); Gregor Mendel Institute of Molecular Plant Biology (GMI); Hallym University; Sungkyunkwan University (SKKU)
• 刊物名称: PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
• ISSN/ISSBN: 0027-9000
• DOI: 10.1073/pnas.2416674122
• 发表日期: 2025-03-11
• 关键词: bud outgrowth; strigolactone; cytokinin; transport; origin; auxin; diversification; metabolism; responses; insights

摘要

Bifacial cambium, which produces xylem and phloem, and monopodial architecture, characterized by apical dominance and lateral branching from axillary buds, are key developmental features of seed plants, consisting of angiosperms and gymnosperms. These allow seed plants to adapt to diverse environments by optimizing resource allocation and structural integrity. In seed plants, SUPPRESSOR OFMAX2-LIKE (SMXL) family members function in phloem development and strigolactone-induced inhibition of axillary bud outgrowth. Although strigolactone signaling regulates most SMXL family members, the only known regulator of SMXL4 and SMXL5 is the RNA-binding protein JULGI. We demonstrate that in angiosperms, by directly regulating SMXL4/5 expression, JULGI uncouples SMXL4/5 activity from strigolactone signaling. JULGI and ancestral SMXLs from seedless vascular plants or SMXL4/5 from seed plants are coexpressed in the phloem tissues of vascular plants, from lycophytes to angiosperms. Core angiosperm SMXL4/5 mRNAs contain a G-rich element in the 5 ' untranslated region (UTR) that serves as a target sequence for JULGI to negatively regulate SMXL4/5 expression. Heterologous expression of JULGIs from various angiosperms rescued the Arabidopsis jul1 jul2 mutant. Expressing SMXL4/5s from seed plants and ancestral SMXLs rescued Arabidopsis smxl4 smxl5. Angiosperm SMXL4/5s lack an RGKT motif for proteasomal degradation. Indeed, treatment with the synthetic strigolactone analog rac-GR24 induced proteasomal degradation of SMXL from ferns and SMXL5a from gymnosperms, but not SMXL4/5 from angiosperms. These findings suggest that in ancestral angiosperms, the 5 ' UTR of SMXL4/5 gained G-rich elements, creating a regulatory module with JULGI that allows the phloem development pathway to act independently of strigolactone signaling.