PRJNA491365
Solanum lycopersicum cultivar:M82 Raw sequence reads
The establishment and maintenance of robustness in biological processes depends on redundancy arising from expanding gene families and the fate of duplicated genes. In plants, the continuous replenishment of stem cells in meristems depends on a conserved feedback circuit involving CLAVATA (CLV) pathway signaling, defined by perception of the CLV3 short signaling peptide by the Leucine-Rich Repeat (LRR) receptor kinase CLV1. In Arabidopsis, stem cell homeostasis is partially buffered by compensation from paralogous receptors when CLV1 is compromised. However, compensation within the large CLV3 peptide family is unclear, and whether similar mechanisms buffer stem cell homeostasis in other species is unknown. Here we show that tomato and Arabidopsis evolved distinct mechanisms to achieve robustness in CLV signaling. In tomato, the phenotypic consequences from loss of CLV3 is partially compensated by dramatic transcriptional upregulation of a paralogous gene. In contrast, Arabidopsis relies on redundancy from multiple CLV3 family members. Peptide compensation in tomato acts primarily through CLV1, whereas peptide redundancy in Arabidopsis requires multiple related receptors. Finally, we find evidence that peptide compensation impacted tomato domestication, yet frequent loss and retention of the CLV3 paralog in the Solanaceae family indicates the evolution of compensation is a dynamic process. Our findings indicate buffering of stem cell homeostasis is a widespread feature in plants and highlight the diverse and transient nature of molecular mechanisms employed to achieve robustness in conserved developmental programs.