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Cited by 13Plant Molecular Biology ResearchPlant-Microbe Interactions and ImmunityChromosomal and Genetic Variations

The DOI matches its Crossref record; 66 of the 66 references it cites were found in a registry or an index.

Differential expansion and retention patterns of LRR‐RLK genes across plant evolution

Open access
Kileeg, Zachary, Haldar, Aparna, Khan, Hasna, Qamar, Arooj, Mott, G. Adam·2023·Plant Direct
DOI 10.1002/pld3.556PMC PMC10739070

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Abstract

To maximize overall fitness, plants must accurately respond to a host of growth, developmental, and environmental signals throughout their life. Many of these internal and external signals are perceived by the leucine‐rich repeat receptor‐like kinases, which play roles in regulating growth, development, and immunity. This largest family of receptor kinases in plants can be divided into subfamilies based on the conservation of the kinase domain, which demonstrates that shared evolutionary history often indicates shared molecular function. Here we investigate the evolutionary history of this family across the evolution of 112 plant species. We identify lineage‐specific expansions of the malectin‐domain containing subfamily LRR subfamily I primarily in the Brassicales and bryophytes. Most other plant lineages instead show a large expansion in LRR subfamily XII, which in Arabidopsis is known to contain key receptors in pathogen perception. This striking asymmetric expansion may reveal a dichotomy in the evolutionary history and adaptation strategies employed by plants. A greater understanding of the evolutionary pressures and adaptation strategies acting on members of this receptor family offers a way to improve functional predictions for orphan receptors and simplify the identification of novel stress‐related receptors.

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Crossref · 10.1002/pld3.556

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Figures

FIGURE 1 Expansion, duplication, and counts of LRR‐RLKs across 112 plant and algae species. (a) The LRR‐RLK subfamily members have undergone asymmetric expansion. Subfamily expansion is represented as the percentage of LRR‐RLKs belonging to each subfamily out of the total number of LRR‐RLKs in each genome. Letters represent the significance group of each subfamily, as determined by Tukey's HSD test at alpha = .05. Subfamilies with shared letters are statistically similar to one another, while subfamilies with different letters are significantly different from one another. Species with less than 10 total LRR‐RLKs were omitted. Subfamilies LRR‐I, LRR‐III, LRR‐VIII, LRR‐XI, and LRR‐XII have a higher proportion of total LRR‐RLKs compared to the other subfamilies, demonstrating increased diversification. (b) LRR‐RLKs have undergone tandem duplication. Blue bars represent tandem duplicated genes, while gray bars represent non‐tandem duplicated genes. Tandem duplicates are those in the same subclade separated on a chromosome by no more than two intervening genes.
FIGURE 1 Expansion, duplication, and counts of LRR‐RLKs across 112 plant and algae species. (a) The LRR‐RLK subfamily members have undergone asymmetric expansion. Subfamily expansion is represented as the percentage of LRR‐RLKs belonging to each subfamily out of the total number of LRR‐RLKs in each genome. Letters represent the significance group of each subfamily, as determined by Tukey's HSD test at alpha = .05. Subfamilies with shared letters are statistically similar to one another, while subfamilies with different letters are significantly different from one another. Species with less than 10 total LRR‐RLKs were omitted. Subfamilies LRR‐I, LRR‐III, LRR‐VIII, LRR‐XI, and LRR‐XII have a higher proportion of total LRR‐RLKs compared to the other subfamilies, demonstrating increased diversification. (b) LRR‐RLKs have undergone tandem duplication. Blue bars represent tandem duplicated genes, while gray bars represent non‐tandem duplicated genes. Tandem duplicates are those in the same subclade separated on a chromosome by no more than two intervening genes.CC BY-NC · PubMed Central
FIGURE 2 Comparison of LRR‐I and LRR‐XII receptor counts across different plant orders. (a) Percentage of total LRR‐RLKs found in subfamilies LRR‐I and LRR‐XII in each given order. Outliers (> Q3 + 1.5xIQR) are plotted as dots. Significance values represent an ANOVA followed by Tukey's HSD. * = p < .05, ** = p < .01, *** = p < .001, **** = p < .0001. (b) LRR‐RLK subfamilies have different ratios of expansion across evolutionary time. Colors indicate the log of the ratio of LRR‐I to LRR‐XII genes at each node. Numbers at terminal nodes represent the ratio for those species and internal nodes represent the ratio for the common ancestor at that branch. Red algae ( P. umbilicalis ) is used as the species outgroup.
FIGURE 2 Comparison of LRR‐I and LRR‐XII receptor counts across different plant orders. (a) Percentage of total LRR‐RLKs found in subfamilies LRR‐I and LRR‐XII in each given order. Outliers (> Q3 + 1.5xIQR) are plotted as dots. Significance values represent an ANOVA followed by Tukey's HSD. * = p < .05, ** = p < .01, *** = p < .001, **** = p < .0001. (b) LRR‐RLK subfamilies have different ratios of expansion across evolutionary time. Colors indicate the log of the ratio of LRR‐I to LRR‐XII genes at each node. Numbers at terminal nodes represent the ratio for those species and internal nodes represent the ratio for the common ancestor at that branch. Red algae ( P. umbilicalis ) is used as the species outgroup.CC BY-NC · PubMed Central
FIGURE 3 Maximum‐likelihood phylogeny of LRR‐I inferred from 112 species of plants and algae based on kinase domain sequences. Outer ring denotes the order in each sequence falls into. Inner ring colors denote the subclade to which each sequence belongs. Bootstrap values represent 1,000 re‐samplings. Subclades were considered as such if sequences shared at least 60% sequence similarity to one another and the subclade contained bootstrap support >90%. Phylogeny was rooted using a variety of Arabidopsis and human kinases. Arabidopsis sequences are marked with red dots, and characterized members are noted.
FIGURE 3 Maximum‐likelihood phylogeny of LRR‐I inferred from 112 species of plants and algae based on kinase domain sequences. Outer ring denotes the order in each sequence falls into. Inner ring colors denote the subclade to which each sequence belongs. Bootstrap values represent 1,000 re‐samplings. Subclades were considered as such if sequences shared at least 60% sequence similarity to one another and the subclade contained bootstrap support >90%. Phylogeny was rooted using a variety of Arabidopsis and human kinases. Arabidopsis sequences are marked with red dots, and characterized members are noted.CC BY-NC · PubMed Central
FIGURE 4 Domain architectures of LRR‐I members across 112 species. (a) General schematic of the two commonly found architectures across 112 species. MLD = malectin‐like domain, LRRs = leucine‐rich repeats, TM = transmembrane domain, GDPC = a cleavage motif, Cys‐pair = predicted disulfide bond, and SP = signal peptide. The two architectures are based on Arabidopsis FRK1 (top) and P. patens receptor Ppate_Pp3c16_23380V3.1.p (bottom). (b) Sequence logo of the WxGDCPxP motif found in the majority of LRR‐I sequences. (c) Uncommon domains found within at least five sequences. Hexagons represent those found within the transmembrane domain, and ovals represent those found within the LRR domain.
FIGURE 4 Domain architectures of LRR‐I members across 112 species. (a) General schematic of the two commonly found architectures across 112 species. MLD = malectin‐like domain, LRRs = leucine‐rich repeats, TM = transmembrane domain, GDPC = a cleavage motif, Cys‐pair = predicted disulfide bond, and SP = signal peptide. The two architectures are based on Arabidopsis FRK1 (top) and P. patens receptor Ppate_Pp3c16_23380V3.1.p (bottom). (b) Sequence logo of the WxGDCPxP motif found in the majority of LRR‐I sequences. (c) Uncommon domains found within at least five sequences. Hexagons represent those found within the transmembrane domain, and ovals represent those found within the LRR domain.CC BY-NC · PubMed Central

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Metadata

Authors
Kileeg, Z., Haldar, A., Khan, H., Qamar, A., & Mott, G. A.
Affiliations
University of Toronto (CA)
Corresponding author
Mott, G. Adam
ORCID
Venue
Plant Direct
Publisher
Wiley
Published
2023-12
Volume
7
Issue
12
Pages
e556-e556
ISSN
2475-4455 (ISSN-L)
DOI
10.1002/pld3.556
PMC
PMC10739070
OpenAlex
W4390110941
Cited by
13
References
66
Citations by year
2026: 2 · 2025: 5 · 2024: 4 · 2023: 2
FWCI
2.04
Type
journal article
Language
en
Open access
Licence
Locations
  • Plant Direct (publishedVersion, cc-by-nc)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by-nc)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
Natural Sciences and Engineering Research Council of Canada
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant-Microbe Interactions and Immunity
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Chromosomal and Genetic Variations
Keywords
leucine-rich repeat receptor-like kinases, gene family expansion, plant evolution, Brassicales, bryophytes, pathogen perception, orphan receptors, plant immunity

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