skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.

Explore Research Products in the PAR
It may take a few hours for recently added research products to appear in PAR search results.


Title: Evolutionary analysis of the LORELEI gene family in plants reveals regulatory subfunctionalization
Abstract A signaling complex comprising members of the LORELEI (LRE)-LIKE GPI-anchored protein (LLG) and Catharanthus roseus RECEPTOR-LIKE KINASE 1-LIKE (CrRLK1L) families perceive RAPID ALKALINIZATION FACTOR (RALF) peptides and regulate growth, reproduction, immunity, and stress responses in Arabidopsis (Arabidopsis thaliana). Genes encoding these proteins are members of multigene families in most angiosperms and could generate thousands of signaling complex variants. However, the links between expansion of these gene families and the functional diversification of this critical signaling complex as well as the evolutionary factors underlying the maintenance of gene duplicates remain unknown. Here, we investigated LLG gene family evolution by sampling land plant genomes and explored the function and expression of angiosperm LLGs. We found that LLG diversity within major land plant lineages is primarily due to lineage-specific duplication events, and that these duplications occurred both early in the history of these lineages and more recently. Our complementation and expression analyses showed that expression divergence (i.e. regulatory subfunctionalization), rather than functional divergence, explains the retention of LLG paralogs. Interestingly, all but one monocot and all eudicot species examined had an LLG copy with preferential expression in male reproductive tissues, while the other duplicate copies showed highest levels of expression in female or vegetative tissues. The single LLG copy in Amborella trichopoda is expressed vastly higher in male compared to in female reproductive or vegetative tissues. We propose that expression divergence plays an important role in retention of LLG duplicates in angiosperms.  more » « less
Award ID(s):
2107215 2023310 2210431
PAR ID:
10382558
Author(s) / Creator(s):
; ; ; ; ; ; ; ; ; ; ; ; ; ; ;
Publisher / Repository:
Oxford University Press
Date Published:
Journal Name:
Plant Physiology
Volume:
190
Issue:
4
ISSN:
0032-0889
Format(s):
Medium: X Size: p. 2539-2556
Size(s):
p. 2539-2556
Sponsoring Org:
National Science Foundation
More Like this
  1. ; ; ; (, G3 Genes|Genomes|Genetics)
    Civetta, A (Ed.)
    Abstract Sexual reproduction in internally fertilizing species requires complex coordination between female and male reproductive systems and among the diverse tissues of the female reproductive tract (FRT). Here, we report a comprehensive, tissue-specific investigation of Drosophila melanogaster FRT gene expression before and after mating. We identified expression profiles that distinguished each tissue, including major differences between tissues with glandular or primarily nonglandular epithelium. All tissues were enriched for distinct sets of genes possessing secretion signals that exhibited accelerated evolution, as might be expected for genes participating in molecular interactions between the sexes within the FRT extracellular environment. Despite robust transcriptional differences between tissues, postmating responses were dominated by coordinated transient changes indicative of an integrated systems-level functional response. This comprehensive characterization of gene expression throughout the FRT identifies putative female contributions to postcopulatory events critical to reproduction and potentially reproductive isolation, as well as the putative targets of sexual selection and conflict. 
    more » « less
  2. ; ; ; ; ; ; (, The Plant Journal)
    SUMMARY The shoot apical meristems (SAMs) of land plants are crucial for plant growth and organ formation. In several angiosperms, theHAIRY MERISTEM(HAM) genes function as key regulators that control meristem development and stem cell homeostasis. To date, the origin and evolutionary history of the HAM family in land plants remains unclear. Potentially shared and divergent functions of HAM family members from angiosperms and non‐angiosperms are also not known. In constructing a comprehensive phylogeny of the HAM family, we show that HAM proteins are widely present in land plants and that HAM proteins originated prior to the divergence of bryophytes. The HAM family was duplicated in a common ancestor of angiosperms, leading to two distinct groups: type I and type II. Type‐II HAM members are widely present in angiosperms, whereas type‐I HAM members were independently lost in different orders of monocots. Furthermore, HAM members from angiosperms and non‐angiosperms (including bryophytes, lycophytes, ferns and gymnosperms) are able to replace the role of the type‐IIHAMgenes in Arabidopsis, maintaining established SAMs and promoting the initiation of new stem cell niches. Our results uncover the conserved functions of HAM family members and reveal the conserved regulatory mechanisms underlying HAM expression patterning in meristems, providing insight into the evolution of key stem cell regulators in land plants. 
    more » « less
  3. ; ; ; (, Molecular Biology and Evolution)
    Wittkopp, Patricia (Ed.)
    Abstract Whole-genome duplications (WGDs) have occurred in many eukaryotic lineages. However, the underlying evolutionary forces and molecular mechanisms responsible for the long-term retention of gene duplicates created by WGDs are not well understood. We employ a population-genomic approach to understand the selective forces acting on paralogs and investigate ongoing duplicate-gene loss in multiple species of Paramecium that share an ancient WGD. We show that mutations that abolish protein function are more likely to be segregating in retained WGD paralogs than in single-copy genes, most likely because of ongoing nonfunctionalization post-WGD. This relaxation of purifying selection occurs in only one WGD paralog, accompanied by the gradual fixation of nonsynonymous mutations and reduction in levels of expression, and occurs over a long period of evolutionary time, “marking” one locus for future loss. Concordantly, the fitness effects of new nonsynonymous mutations and frameshift-causing indels are significantly more deleterious in the highly expressed copy compared with their paralogs with lower expression. Our results provide a novel mechanistic model of gene duplicate loss following WGDs, wherein selection acts on the sum of functional activity of both duplicate genes, allowing the two to wander in expression and functional space, until one duplicate locus eventually degenerates enough in functional efficiency or expression that its contribution to total activity is too insignificant to be retained by purifying selection. Retention of duplicates by such mechanisms predicts long times to duplicate-gene loss, which should not be falsely attributed to retention due to gain/change in function. 
    more » « less
  4. ; ; ; ; ; ; ; ; ; ; et al (, Molecular Ecology)
    Abstract Early lineage diversification is central to understand what mutational events drive species divergence. Particularly, gene misregulation in interspecific hybrids can inform about what genes and pathways underlie hybrid dysfunction. InDrosophilahybrids, how regulatory evolution impacts different reproductive tissues remains understudied. Here, we generate a new genome assembly and annotation inDrosophila willistoniand analyse the patterns of transcriptome divergence between two allopatrically evolvedD. willistonisubspecies, their male sterile and female fertile hybrid progeny across testis, male accessory gland, and ovary. Patterns of transcriptome divergence and modes of regulatory evolution were tissue‐specific. Despite no indication for cell‐type differences in hybrid testis, this tissue exhibited the largest magnitude of expression differentiation between subspecies and between parentals and hybrids. No evidence for anomalous dosage compensation in hybrid male tissues was detected nor was a differential role for the neo‐ and the ancestral arms of theD. willistoni Xchromosome. Compared to the autosomes, theXchromosome appeared enriched for transgressively expressed genes in testis despite being the least differentiated in expression between subspecies. Evidence for fine genome clustering of transgressively expressed genes suggests a role of chromatin structure on hybrid gene misregulation. Lastly, transgressively expressed genes in the testis of the sterile male progeny were enriched for GO terms not typically associated with sperm function, instead hinting at anomalous development of the reproductive tissue. Our thorough tissue‐level portrait of transcriptome differentiation between recently divergedD. willistonisubspecies and their hybrids provides a more nuanced view of early regulatory changes during speciation. 
    more » « less
  5. ; ; ; ; ; ; ; (, Plant Physiology)
    Abstract The Arabidopsis (Arabidopsis thaliana) BYPASS1 (BPS1) gene encodes a protein with no functionally characterized domains, and loss-of-function mutants (e.g. bps1-2 in Col-0) present a severe growth arrest phenotype that is evoked by a root-derived graft-transmissible small molecule that we call dalekin. The root-to-shoot nature of dalekin signaling suggests it could be an endogenous signaling molecule. Here, we report a natural variant screen that allowed us to identify enhancers and suppressors of the bps1-2 mutant phenotype (in Col-0). We identified a strong semi-dominant suppressor in the Apost-1 accession that largely restored shoot development in bps1 and yet continued to overproduce dalekin. Using bulked segregant analysis and allele-specific transgenic complementation, we showed that the suppressor is the Apost-1 allele of a BPS1 paralog, BYPASS2 (BPS2). BPS2 is one of four members of the BPS gene family in Arabidopsis, and phylogenetic analysis demonstrated that the BPS family is conserved in land plants and the four Arabidopsis paralogs are retained duplicates from whole genome duplications. The strong conservation of BPS1 and paralogous proteins throughout land plants, and the similar functions of paralogs in Arabidopsis, suggests that dalekin signaling might be retained across land plants. 
    more » « less
  • Citation Formats
  • MLA
  • APA
  • Chicago
  • BibTeX
  • Save / Share this Record
  • Send to Email