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Proc. Natl. Acad. Sci. USA, Mar 11 2025, 122 (10) | https://doi.org/10.1073/pnas.2416674122 Evolution of the JULGI-SMXL4/5 module for phloem development in angiosperms

Chanyoung Park ¹, Hyun Seob Cho ¹, Yookyung Lim ², Chung Hyun Cho ³, Hoyoung Nam ¹, Sangkyu Choi ¹, Hojun Lim ¹, Young-Dong Kim ⁴, Hwan Su Yoon ⁵, Hyunwoo Cho ², Ildoo Hwang ^{1 *}

¹Department of Life Sciences, Pohang University of Science and Technology, Pohang 37673, Korea.
²Department of Industrial Plant Science and Technology, Chungbuk National University, Cheongju 28644, Korea.
³Gregor Mendel Institute, Austrian Academy of Sciences, Vienna BioCenter, Vienna 1030, Austria.
⁴Department of Life Sciences, Hallym University, Chuncheon 24252, Korea.
⁵Department of Biological Science, Sungkyunkwan University, Suwon 16419, Korea.

^*Corresponding author: correspondence to Ildoo Hwang

Abstract

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 OF MAX2-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.

논문정보

형식Research article
게재일2025년 03월 (BRIC 등록일 2025-03-10)
연구진국내(교신)+국외 연구진
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