Extreme restructuring of cis-regulatory regions controlling a deeply conserved plant stem cell regulator

Ciren, Danielle, Zebell, Sophia, Lippman, Zachary B (March 2024) Extreme restructuring of cis-regulatory regions controlling a deeply conserved plant stem cell regulator. PLoS Genetics, 20 (3). e1011174. ISSN 1553-7390

PDF journal.pgen.1011174.pdf - Published Version Available under License Creative Commons Attribution. Download (3MB)

Abstract

A striking paradox is that genes with conserved protein sequence, function and expression pattern over deep time often exhibit extremely divergent cis-regulatory sequences. It remains unclear how such drastic cis-regulatory evolution across species allows preservation of gene function, and to what extent these differences influence how cis-regulatory variation arising within species impacts phenotypic change. Here, we investigated these questions using a plant stem cell regulator conserved in expression pattern and function over ~125 million years. Using in-vivo genome editing in two distantly related models, Arabidopsis thaliana (Arabidopsis) and Solanum lycopersicum (tomato), we generated over 70 deletion alleles in the upstream and downstream regions of the stem cell repressor gene CLAVATA3 (CLV3) and compared their individual and combined effects on a shared phenotype, the number of carpels that make fruits. We found that sequences upstream of tomato CLV3 are highly sensitive to even small perturbations compared to its downstream region. In contrast, Arabidopsis CLV3 function is tolerant to severe disruptions both upstream and downstream of the coding sequence. Combining upstream and downstream deletions also revealed a different regulatory outcome. Whereas phenotypic enhancement from adding downstream mutations was predominantly weak and additive in tomato, mutating both regions of Arabidopsis CLV3 caused substantial and synergistic effects, demonstrating distinct distribution and redundancy of functional cis-regulatory sequences. Our results demonstrate remarkable malleability in cis-regulatory structural organization of a deeply conserved plant stem cell regulator and suggest that major reconfiguration of cis-regulatory sequence space is a common yet cryptic evolutionary force altering genotype-to-phenotype relationships from regulatory variation in conserved genes. Finally, our findings underscore the need for lineage-specific dissection of the spatial architecture of cis-regulation to effectively engineer trait variation from conserved productivity genes in crops.

Item Type:	Paper
Subjects:	organism description > plant > Arabidopsis organism description > plant behavior organs, tissues, organelles, cell types and functions > cell types and functions > cell types organs, tissues, organelles, cell types and functions > cell types and functions > cell types organs, tissues, organelles, cell types and functions > cell types and functions > cell types organs, tissues, organelles, cell types and functions > cell types and functions organism description > plant behavior > crop yield improvement organs, tissues, organelles, cell types and functions organism description > plant organs, tissues, organelles, cell types and functions > cell types and functions > cell types > stem cells organs, tissues, organelles, cell types and functions > cell types and functions > cell types > stem cells organs, tissues, organelles, cell types and functions > cell types and functions > cell types > stem cells
CSHL Authors:	Ciren, Danielle Zebell, Sophia G. Lippman, Zachary B.
Communities:	CSHL labs > Lippman lab
SWORD Depositor:	CSHL Elements
Depositing User:	CSHL Elements
Date:	4 March 2024
Date Deposited:	07 Mar 2024 18:20
Last Modified:	07 Mar 2024 18:20
PMCID:	PMC10911594
Related URLs:	Publisher
URI:	https://repository.cshl.edu/id/eprint/41455

Actions (login required)

Administrator's edit/view item