Robil, Janlo M.

archīum.ATENEO (Ateneo de Manila Univ.)

Ateneo de Manila University Archīum Ateneo Biology Faculty Publications Biology Department 12-1-2023 The Many Side Jobs of Lateral suppressor (Ls) in Plant Development Janlo M. Robil Ateneo de Manila University Follow this and additional works at: https://archium.ateneo.edu/biology-faculty-pubs  Part of the Physiology Commons, and the Plant Sciences Commons Recommended Citation Robil JM. The many side jobs of Lateral suppressor (Ls) in plant development. Plant Physiol. 2023 Nov 22;193(4):2254-2256. doi: 10.1093/plphys/kiad496. PMID: 37706552; PMCID: PMC10663106. This Article is brought to you for free and open access by the Biology Department at Archīum Ateneo. It has been accepted for inclusion in Biology Faculty Publications by an authorized administrator of Archīum Ateneo. For more information, please contact oadrcw.ls@ateneo.edu. The many side jobs of Lateral suppressor (Ls) in plant developmentJanlo M. Robil 1,2,*1 Assistant Features Editor, Plant Physiology, American Society of Plant Biologists2 Department of Biology, School of Science and Engineering, Ateneo de Manila University, Quezon City 1108, Philippines *Author for correspondence: jrobil@ateneo.eduNews and Views Received August 14, 2023. Accepted August 22, 2023. Advance access publication September 14, 2023 Open Access © The Author(s) 2023. Published by Oxford University Press on behalf of American Society of Plant Biologists. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.Shoot architecture in plants is defined by the formation and specification of branches. For millennia, humans have been selecting crop plants based on shoot architecture that favors optimal performance and yield. In recent decades, several genes have been identified to control branch initiation, growth, and determinacy. Among these genes, Lateral sup-pressor (Ls), a GRAS transcription factor, affects branching in diverse plants, including tomato, rice, and Arabidopsis (Schumacher et al. 1999; Greb et al. 2003; Li et al. 2003). Mutations in the Ls gene and its co-orthologs result in a dra-matic reduction in branch or tiller number due to repressed activity of the axillary meristems (AMs). The Ls gene is a promising target for crop engineering, but species-specific developmental effects complicate the understanding of its mechanisms (Wang et al. 2018). Therefore, a detailed inves-tigation of the regulatory mechanisms of Ls across species and developmental contexts is essential.In this issue of Plant Physiology, Jiang et al. (2023) expand our understanding of Ls in commercial watermelon (Citrullus lanatus). They found that, in addition to promoting axillary organ formation, Cl Lateral suppressor (ClLs) also con-trols tendril and flower identities and leaf morphology (Fig.). Genetic and molecular evidence suggests that sub- functionalization of ClLs in watermelon is likely mediated by ClLs interacting with different protein partners, support-ing a broader involvement of Ls in key developmental path-ways in plants.The wild-type watermelon has multiple branches, many of which are modified into tendrils, the threadlike structure that facilitates the plant’s clinging habit. The branches, ten-drils, and flowers all develop from the axils of the leaves, which are characterized by their lobed leaf blades. In order to determine its role in axillary organ development, the authors generated CRISPR/CAS9-mediated knockouts of ClLs. All knockout lines lack branches, tendrils, and flowers, and their leaves appear round due to the absence of lobula-tion. Those mutant phenotypes support the functional con-servation of Ls in eudicots but also reveal a previously uncharacterized role of the gene in leaf development.Jiang et al. (2023) investigated whether the functional ex-pansion in ClLs is determined by choosing different protein partners, given that LS has been shown to interact with other proteins to control AM formation (Raman et al. 2008; Rossmann et al. 2015; Guo et al. 2021). First, Jiang et al. (2023) performed a yeast 2-hybrid screen of the wild-type shoot apex and found multiple putative ClLS-interacting partners, including a TCP transcription factor (ClTEN), a ser-ine/threonine kinase (ClPID), and a MADS-box transcription factor (ClAP1). They then conducted a series of in vivo and in vitro assays, all of which show physical interaction of ClLS with those 3 proteins. The new interacting partners for ClLS could potentially help explain its sub-functionalization in watermelon.In order to test whether there are overlapping gene activ-ities between ClLs and ClTEN, ClPID, and ClAP1, the authors investigated their mRNA expression patterns in the develop-ing shoot apices by in situ hybridization. As expected, ClLs is expressed in the axils of the AMs and leaf primordia. However, in the leaf primordia, ClLs is also expressed in nar-row regions of the future leaf blade. Of the 3 interacting genes, only ClPID shares similar expression domains with ClLs. In contrast, both ClTEN and ClAP1 are exclusively https://doi.org/10.1093/plphys/kiad496 PLANT PHYSIOLOGY 2023: 193: 2254–2256Downloaded from https://academic.oup.com/plphys/article/193/4/2254/7273627 by guest on 19 February 2024expressed in the AMs that correspond to incipient tendril primordia and floral meristems, respectively. Those observa-tions suggest that ClLs and ClPID have overlapping gene activ-ities in the axils and developing leaves. On the other hand, the expression of ClTEN and ClAP1 in AMs, where ClLs is excluded, suggests antagonistic gene activities and raises interesting questions about their regulatory mechanisms.Finally, to further investigate the functions of ClTEN, ClPID, and ClAP1, Jiang et al. (2023) generated knockout lines of each gene with CRISPR/Cas9. In Clten mutants, tendrils are either absent or replaced by branches that exhibit tendril-like curvatures. Clpid mutants exhibit a dwarf and compact stat-ure, produce flowers with missing lateral organs, and have notably rounder leaves that lack lobes. Although Clap1 mu-tants exhibit normal vegetative structures, they completely fail to produce flowers throughout their development. In addition, the authors found that the transcript levels of ClLs were significantly reduced in all those knockout lines. Altogether, Clten, Clpid, and Clap1 mutants recapitulate dis-tinct phenotypes observed in ClLs mutants, providing further evidence for overlapping functions of those 3 genes with ClLs in the patterning lateral organs in watermelon.The authors conclude that ClLs had undergone sub- functionalization in watermelon, with ClLS protein interact-ing with ClTEN, ClPID, and ClAP1 proteins to control the de-velopment of tendrils, leaves, and flowers, respectively (Fig.). However, further analysis is needed to understand the specif-ic mechanisms of those interactions. For example, it will be important to determine whether ClPID phosphorylates ClLS. Additionally, since the expression domains of ClTEN and ClAP1 do not overlap with those of ClLs, it will be import-ant to investigate whether these proteins interact with ClLs through non-cell autonomous signaling. Moreover, future studies should clarify the roles of auxin, gibberellic acid, and strigolactones in ClLs sub-functionalization, based on the known relationships of its interacting proteins with these hormones (Wang et al. 2018).The work of Jiang et al. (2023) has implications for crop breeding as it highlights the challenges and limitations of tar-geting a single gene to modify plant architecture. The long- term goal of the study was to improve watermelon fruit har-vesting efficiency by reducing multiple branching, but the unintended effects of disabling ClLs on the development of other vegetative and reproductive organs underscore the complexity of the precise mechanisms controlling axillary or-gan formation. Yet, the study reveals new and important in-formation about the diverse functions of Ls, which could pave the way for improving shoot architecture in water-melon and other crop species.Conflict of interest statement. None declared.ReferencesGreb T, Clarenz O, Schäfer E, Müller D, Herrero R, Schmitz G, Theres K. Molecular analysis of the LATERAL SUPPRESSOR gene in Arabidopsis reveals a conserved control mechanism for axillary meri-stem formation. Genes Dev. 2003:17(9):1175–1187. https://doi.org/ 10.1101/gad.260703ClLsClTENClPIDClAP1ClLSClTENClLSClPIDClLSClAP1LPAMSAMtendril formationleaf lobulationfloral initiationA BFigure. Control of lateral organ patterning in watermelon by Citrullus lanatus Lateral suppressor (ClLs) through interaction with protein partners. A) mRNA expression patterns of ClLs, ClTEN, ClPID, and ClAP1 in the shoot apex of wild-type watermelon. B) ClLS protein physically interacts with ClTEN, ClPID, and ClAP1 to regulate tendril formation, leaf lobulation, and floral initiation. AM, axillary meristem; LP, leaf primordium; SAM, shoot apical meristem.Control of lateral organ patterning in watermelon                                                   PLANT PHYSIOLOGY 2023: 193; 2254–2256 | 2255Downloaded from https://academic.oup.com/plphys/article/193/4/2254/7273627 by guest on 19 February 2024Guo M, Long Y, Xu L, Zhang W, Liu T, Zhang C, Hou X, Li Y. Cell cycle SEITCH 52 regulates tillering by interacting with LATERAL SUPPRESSOR in non-heading Chinese cabbage. Plant Sci. 2021:309: 110934. https://doi.org/10.1016/j.plantsci.2021.110934Jiang Y, Zhang A, He W, Li Q, Zhao B, Zhao H, Ke X, Guo Y, Sun P, Yang T, et al. GRAS family member LATERAL SUPPRESSOR regulates the initiation and morphogenesis of watermelon lateral organs. Plant Physiol. 2023:193(4):2592–2604. https://doi.org/10.1093/ plphys/kiad445Li X, Qian Q, Fu Z, Wang Y, Xiong G, Zeng D, Wang X, Liu X, Teng S, Hiroshi F, et al. Control of tillering in rice. Nature. 2003:422(6932): 618–621. https://doi.org/10.1038/nature01518Raman S, Greb T, Peaucelle A, Blein T, Laufs P, Theres K. Interplay of miR164, CUP-SHAPED COTYLEDON genes and LATERAL SUPPRESSOR controls axillary meristem formation in Arabidopsis thaliana. Plant J. 2008:55(1):65–76. https://doi.org/10.1111/j.1365- 313X.2008.03483.xRossmann S, Kohlen W, Hasson A, Theres K. Lateral suppressor and Goblet act in hierarchical order to regulate ectopic meristem forma-tion at the base of tomato leaflets. Plant J. 2015:81(6):837–848. https://doi.org/10.1111/tpj.12782Schumacher K, Schmitt T, Rossberg M, Schmitz G, Theres K. The Lateral suppressor (Ls) gene of tomato encodes a new member of the VHIID protein family. Proc Natl Acad Sci USA. 1999:96(1): 290–295. https://doi.org/10.1073/pnas.96.1.290Wang B, Smith SM, Li J. Genetic regulation of shoot architecture. Annu Rev Plant Biol. 2018:69(1):437–468. https://doi.org/10.1146/annurev- arplant-042817-0404222256 | PLANT PHYSIOLOGY 2023: 193; 2254–2256                                                                                                                    RobilDownloaded from https://academic.oup.com/plphys/article/193/4/2254/7273627 by guest on 19 February 2024

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The Many Side Jobs of Lateral suppressor (Ls) in Plant Development

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