Evolutionary conservation of receptor compensation for stem cell homeostasis in Solanaceae plants

Abstract

Stem cell homeostasis is pivotal for continuous and programmed formation of organs in plants. The precise control of meristem proliferation is mediated by the evolutionarily conserved signaling that encompasses complex interactions among multiple peptide ligands and their receptor-like kinases. Here, we identified compensation mechanisms involving the CLAVATA1 (CLV1) receptor and its paralogs, BARELY ANY MERISTEMs (BAMs), for stem cell proliferation in two Solanaceae species, tomato and groundcherry. Genetic analyses of higher-order mutants deficient in multiple receptor genes, generated via CRISPR-Cas9 genome editing, reveal that tomato SlBAM1 and SlBAM2 compensate for slclv1 mutations. Unlike the compensatory responses between orthologous receptors observed in Arabidopsis, tomato slclv1 mutations do not trigger transcriptional upregulation of four SlBAM genes. The compensation mechanisms within receptors are also conserved in groundcherry, and critical amino acid residues of the receptors associated with the physical interaction with peptide ligands are highly conserved in Solanaceae plants. Our findings demonstrate that the evolutionary conservation of both compensation mechanisms and critical coding sequences between receptor-like kinases provides a strong buffering capacity during stem cell homeostasis in tomato and groundcherry.

Acknowledgements

We regret the absence of additional citations, adhering to the author guidelines that prescribe a more limited number of references. We thank all members of the Kwon lab at Kyung Hee University for comments, discussions, and assistance with plant care; all members of the Lippman lab from Cold Spring Harbor Laboratory for comments and discussions; T. Mulligan, K. Schlecht, A. Krainer, and S. Qiao from Cold Spring Harbor Laboratory for assistance with plant care; J. Van Eck, A. Horowitz Doyle, K. Swartwood, M. Tjahjadi, L. Randall, and P. Keen from Boyce Thompson Institute for assistance with the tomato and groundcherry transformations. This research was funded by the National Research Foundation (NRF) of the Ministry of Science and ICT (MSIT), Republic of Korea (No. 2022R1C1C1002941 to C.-T.K., No. 2020R1A2C1101915 to S.J.P., and No. RS-2023-00217064 to W.-J.H.), the Howard Hughes Medical Institute, and the National Science Foundation Plant Genome Research Program (No. IOS-1732253) to Z.B.L.

Author contributions

M.-G.S. and Y.L. performed the experiments and edited the manuscript. A.H. and G.R. performed the groundcherry experiments. H.K.B. performed the tomato experiments. W.-J.H. performed the phylogenetic analysis. S.J.P. generated transgenic tomato plants and performed the tomato experiments. Z.B.L. conceived the research and supervised the experiments. Y.-J.P. performed the experiments, prepared the figures, and wrote the manuscript. C.-T.K. conceived and led the research, supervised and performed the experiments, prepared the figures, and wrote the manuscript. All authors read and approved the manuscript.

Supplementary Data

Supplementary data is available at Horticulture Research online.

Conflict of interest statement

The authors declare that they have no conflict of interest.

Data availability

Raw data and information for CRISPR-generated alleles, all quantifications, and exact P values (one-way ANOVA and Tukey test) are in Supplementary Table S6. The raw Sanger sequence traces for edited sequences are in Supplementary Data Files. The tomato and groundcherry BioProject accession numbers are PRJNA491365, PRJNA704671, and PRJNA862958.

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