Balancing selection on an MYB transcription factor maintains the twig trichome color variation in Melastoma normale

Abstract Background The factors that maintain phenotypic and genetic variation within a population have received long-term attention in evolutionary biology. Here the genetic basis and evolution of the geographically widespread variation in twig trichome color (from red to white) in a shrub Melastom...

Full description

Bibliographic Details
Main Authors: Guilian Huang, Wei Wu, Yongmei Chen, Xueke Zhi, Peishan Zou, Zulin Ning, Qiang Fan, Ying Liu, Shulin Deng, Kai Zeng, Renchao Zhou
Format: Article
Language:English
Published: BMC 2023-05-01
Series:BMC Biology
Subjects:
Online Access:https://doi.org/10.1186/s12915-023-01611-4
_version_ 1797817752517345280
author Guilian Huang
Wei Wu
Yongmei Chen
Xueke Zhi
Peishan Zou
Zulin Ning
Qiang Fan
Ying Liu
Shulin Deng
Kai Zeng
Renchao Zhou
author_facet Guilian Huang
Wei Wu
Yongmei Chen
Xueke Zhi
Peishan Zou
Zulin Ning
Qiang Fan
Ying Liu
Shulin Deng
Kai Zeng
Renchao Zhou
author_sort Guilian Huang
collection DOAJ
description Abstract Background The factors that maintain phenotypic and genetic variation within a population have received long-term attention in evolutionary biology. Here the genetic basis and evolution of the geographically widespread variation in twig trichome color (from red to white) in a shrub Melastoma normale was investigated using Pool-seq and evolutionary analyses. Results The results show that the twig trichome coloration is under selection in different light environments and that a 6-kb region containing an R2R3 MYB transcription factor gene is the major region of divergence between the extreme red and white morphs. This gene has two highly divergent groups of alleles, one of which likely originated from introgression from another species in this genus and has risen to high frequency (> 0.6) within each of the three populations under investigation. In contrast, polymorphisms in other regions of the genome show no sign of differentiation between the two morphs, suggesting that genomic patterns of diversity have been shaped by homogenizing gene flow. Population genetics analysis reveals signals of balancing selection acting on this gene, and it is suggested that spatially varying selection is the most likely mechanism of balancing selection in this case. Conclusions This study demonstrate that polymorphisms on a single transcription factor gene largely confer the twig trichome color variation in M. normale, while also explaining how adaptive divergence can occur and be maintained in the face of gene flow.
first_indexed 2024-03-13T08:58:06Z
format Article
id doaj.art-2080018535a545129cd4b66276595fa0
institution Directory Open Access Journal
issn 1741-7007
language English
last_indexed 2024-03-13T08:58:06Z
publishDate 2023-05-01
publisher BMC
record_format Article
series BMC Biology
spelling doaj.art-2080018535a545129cd4b66276595fa02023-05-28T11:27:37ZengBMCBMC Biology1741-70072023-05-0121111910.1186/s12915-023-01611-4Balancing selection on an MYB transcription factor maintains the twig trichome color variation in Melastoma normaleGuilian Huang0Wei Wu1Yongmei Chen2Xueke Zhi3Peishan Zou4Zulin Ning5Qiang Fan6Ying Liu7Shulin Deng8Kai Zeng9Renchao Zhou10State Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-Sen UniversityState Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-Sen UniversityCollege of Chemical Engineering, Sichuan University of Science & EngineeringState Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-Sen UniversityState Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-Sen UniversityGuangdong Provincial Key Laboratory of Applied Botany, South China Botanical Garden, Chinese Academy of SciencesState Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-Sen UniversityState Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-Sen UniversityGuangdong Provincial Key Laboratory of Applied Botany, South China Botanical Garden, Chinese Academy of SciencesDepartment of Animal and Plant Sciences, University of SheffieldState Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-Sen UniversityAbstract Background The factors that maintain phenotypic and genetic variation within a population have received long-term attention in evolutionary biology. Here the genetic basis and evolution of the geographically widespread variation in twig trichome color (from red to white) in a shrub Melastoma normale was investigated using Pool-seq and evolutionary analyses. Results The results show that the twig trichome coloration is under selection in different light environments and that a 6-kb region containing an R2R3 MYB transcription factor gene is the major region of divergence between the extreme red and white morphs. This gene has two highly divergent groups of alleles, one of which likely originated from introgression from another species in this genus and has risen to high frequency (> 0.6) within each of the three populations under investigation. In contrast, polymorphisms in other regions of the genome show no sign of differentiation between the two morphs, suggesting that genomic patterns of diversity have been shaped by homogenizing gene flow. Population genetics analysis reveals signals of balancing selection acting on this gene, and it is suggested that spatially varying selection is the most likely mechanism of balancing selection in this case. Conclusions This study demonstrate that polymorphisms on a single transcription factor gene largely confer the twig trichome color variation in M. normale, while also explaining how adaptive divergence can occur and be maintained in the face of gene flow.https://doi.org/10.1186/s12915-023-01611-4Genetic basisBalancing selectionColor variationIntrogressionMelastoma
spellingShingle Guilian Huang
Wei Wu
Yongmei Chen
Xueke Zhi
Peishan Zou
Zulin Ning
Qiang Fan
Ying Liu
Shulin Deng
Kai Zeng
Renchao Zhou
Balancing selection on an MYB transcription factor maintains the twig trichome color variation in Melastoma normale
BMC Biology
Genetic basis
Balancing selection
Color variation
Introgression
Melastoma
title Balancing selection on an MYB transcription factor maintains the twig trichome color variation in Melastoma normale
title_full Balancing selection on an MYB transcription factor maintains the twig trichome color variation in Melastoma normale
title_fullStr Balancing selection on an MYB transcription factor maintains the twig trichome color variation in Melastoma normale
title_full_unstemmed Balancing selection on an MYB transcription factor maintains the twig trichome color variation in Melastoma normale
title_short Balancing selection on an MYB transcription factor maintains the twig trichome color variation in Melastoma normale
title_sort balancing selection on an myb transcription factor maintains the twig trichome color variation in melastoma normale
topic Genetic basis
Balancing selection
Color variation
Introgression
Melastoma
url https://doi.org/10.1186/s12915-023-01611-4
work_keys_str_mv AT guilianhuang balancingselectiononanmybtranscriptionfactormaintainsthetwigtrichomecolorvariationinmelastomanormale
AT weiwu balancingselectiononanmybtranscriptionfactormaintainsthetwigtrichomecolorvariationinmelastomanormale
AT yongmeichen balancingselectiononanmybtranscriptionfactormaintainsthetwigtrichomecolorvariationinmelastomanormale
AT xuekezhi balancingselectiononanmybtranscriptionfactormaintainsthetwigtrichomecolorvariationinmelastomanormale
AT peishanzou balancingselectiononanmybtranscriptionfactormaintainsthetwigtrichomecolorvariationinmelastomanormale
AT zulinning balancingselectiononanmybtranscriptionfactormaintainsthetwigtrichomecolorvariationinmelastomanormale
AT qiangfan balancingselectiononanmybtranscriptionfactormaintainsthetwigtrichomecolorvariationinmelastomanormale
AT yingliu balancingselectiononanmybtranscriptionfactormaintainsthetwigtrichomecolorvariationinmelastomanormale
AT shulindeng balancingselectiononanmybtranscriptionfactormaintainsthetwigtrichomecolorvariationinmelastomanormale
AT kaizeng balancingselectiononanmybtranscriptionfactormaintainsthetwigtrichomecolorvariationinmelastomanormale
AT renchaozhou balancingselectiononanmybtranscriptionfactormaintainsthetwigtrichomecolorvariationinmelastomanormale