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.2021 Jun 24;127(7):887-902.
doi: 10.1093/aob/mcab028.

Genome size evolution is associated with climate seasonality and glucosinolates, but not life history, soil nutrients or range size, across a clade of mustards

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Genome size evolution is associated with climate seasonality and glucosinolates, but not life history, soil nutrients or range size, across a clade of mustards

N Ivalú Cacho et al. Ann Bot..

Abstract

Background and aims: We investigate patterns of evolution of genome size across a morphologically and ecologically diverse clade of Brassicaceae, in relation to ecological and life history traits. While numerous hypotheses have been put forward regarding autecological and environmental factors that could favour small vs. large genomes, a challenge in understanding genome size evolution in plants is that many hypothesized selective agents are intercorrelated.

Methods: We contribute genome size estimates for 47 species of Streptanthus Nutt. and close relatives, and take advantage of many data collections for this group to assemble data on climate, life history, soil affinity and composition, geographic range and plant secondary chemistry to identify simultaneous correlates of variation in genome size in an evolutionary framework. We assess models of evolution across clades and use phylogenetically informed analyses as well as model selection and information criteria approaches to identify variables that can best explain genome size variation in this clade.

Key results: We find differences in genome size and heterogeneity in its rate of evolution across subclades of Streptanthus and close relatives. We show that clade-wide genome size is positively associated with climate seasonality and glucosinolate compounds. Model selection and information criteria approaches identify a best model that includes temperature seasonality and fraction of aliphatic glucosinolates, suggesting a possible role for genome size in climatic adaptation or a role for biotic interactions in shaping the evolution of genome size. We find no evidence supporting hypotheses of life history, range size or soil nutrients as forces shaping genome size in this system.

Conclusions: Our findings suggest climate seasonality and biotic interactions as potential forces shaping the evolution of genome size and highlight the importance of evaluating multiple factors in the context of phylogeny to understand the effect of possible selective agents on genome size.

Keywords: Streptanthus; Brassicaceae; climate; glucosinolates; plant defence; range size; seasonality; soil chemistry.

© The Author(s) 2021. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.

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Figures

Fig. 1.
Fig. 1.
Genome size inStreptanthus and close relatives, adjusted for recent polyploidy (log 2Cx values), mapped onto the maximum credibility tree of a 50 million generation Bayesian analysis (Cachoet al., 2014) using function ‘contmap’ from R library ‘phytools’ (Revell, 2012). A phylogenetic ANOVA (inset) supports smaller genomes for core streptanthoids (Streptanthus clade I + Guillenia clade) compared with the rest of the species (function ‘aov.phylo’, ‘geiger’ package, Harmonet al., 2008). For genome size estimates and chromosome counts, see Appendix 1. For phylogenetic signal estimates, see Supplementary data Table S1. Genera are abbreviated as follows: C = Caulanthus, S = Streptanthus, Si = Sibaropsis, Sl = Streptanthella, St = Stanleya, The = Thyelypodium.
Fig. 2.
Fig. 2.
Genome size in relation to investment in climatic and defence variables forStreptanthus and relatives. Taking phylogeny into account, genome size in this group correlates negatively with climate PC1 (A). Genome size has a positive association with temperature (T) seasonality (B) and temperature annual range (C), and a negative one with precipitation (P) seasonality (D). Smaller genomes are associated with a larger fraction of aliphatic glucosinolates (E) and also a smaller overall number of glucosinolate compounds (glucosinolate richness, F). Temperature seasonality and fraction of aliphatic glucosinolates are in all best models explaining genome size. Dotted lines represent phylogenetic generalized least squares (PGLS) model fit using the maximum clade credibility tree of a 50 million generation Bayesian analysis (Cachoet al., 2014). For PGLS estimates across a sample of trees and best models, see Tables 2–4 and Supplementary data Table S8.
Fig. 3.
Fig. 3.
Genome size inStreptanthus and close relatives tends to be smaller in environments with moderate temperature seasonality, such as those in the California Floristic Province, and larger in more seasonal continental areas when phylogeny is taken into account. In the figure, the top panel (A) illustrates species in California and adjacent Nevada, the line inset (B) illustrates the eastern area where species occur in New Mexico, Texas and Oklahoma (C). Each circle is plotted at the geographic centre of a species range, for lineages included in our analyses. Circle size on the map corresponds to standardized 2Cx genome size of a species to better visualize differences on the landscape, and circle colours correspond to major clades (see key and Fig. 1). Species: (1)C. amplexicaulis, (2)C. anceps, (3)C. californicus, (4)C. cooperi, (5)C. crassicaulis, (6)C. glaucus, (7)C. hallii, (8)C. heterophyllus, (9)C. inflatus, (10)C. lemmonii, (11)C. pilosus, (12)C. simulans, (13)C. flavescens, (14)C. lasiophyllus, (15)S. albidus, (16)S. barbatus, (17)S. barbiger, (18)S. batrachopus, (19)S. bernardinus, (20)S. brachiatus, (21)S. bracteatus, (22)S. breweri, (23)S. callistus, (24)S. carinatus, (25)S. cordatus, (26)S. diversifolius, (27)S. drepanoides, (28)S. farnsworthianus, (29)S. glandulosus_C1, (30)S. glandulosus_C2, (31)S. glandulosus_C3, (32)S. hesperidis, (33)S. hispidus, (34)S. howellii, (35)S. hyacinthoides, (36)S. insignis, (37)S. longisiliquus, (38)S. morrisonii, (39)S. polygaloides, (40)S. tortuosus, (41)S. vernalis, (42)Si. hammittii, (43)Sl. longirostris, (44)St. elata, (45)St. pinnata, (46)The. laciniatum. Genera are abbreviated as follows: C = Caulanthus, S = Streptanthus, Si = Sibaropsis, Sl = Streptanthella, St = Stanleya, The = Thelypodium.
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