Different evolutionary patterns of TIR1/AFBs and AUX/IAAs and their implications for the morphogenesis of land plants

Abstract Background The plant hormone auxin is widely involved in plant growth, development, and morphogenesis, and the TIR1/AFB and AUX/IAA proteins are closely linked to rapid auxin response and signal transmission. However, their evolutionary history, historical patterns of expansion and contract...

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Main Authors: Liyao Su, Tian Zhang, Bin Yang, Tianyu Dong, Xiaoyu Liu, Yibo Bai, Hui Liu, Jingsong Xiong, Yan Zhong, Zong-Ming (Max) Cheng
Format: Article
Language:English
Published: BMC 2023-05-01
Series:BMC Plant Biology
Subjects:
Online Access:https://doi.org/10.1186/s12870-023-04253-4
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author Liyao Su
Tian Zhang
Bin Yang
Tianyu Dong
Xiaoyu Liu
Yibo Bai
Hui Liu
Jingsong Xiong
Yan Zhong
Zong-Ming (Max) Cheng
author_facet Liyao Su
Tian Zhang
Bin Yang
Tianyu Dong
Xiaoyu Liu
Yibo Bai
Hui Liu
Jingsong Xiong
Yan Zhong
Zong-Ming (Max) Cheng
author_sort Liyao Su
collection DOAJ
description Abstract Background The plant hormone auxin is widely involved in plant growth, development, and morphogenesis, and the TIR1/AFB and AUX/IAA proteins are closely linked to rapid auxin response and signal transmission. However, their evolutionary history, historical patterns of expansion and contraction, and changes in interaction relationships are still unknown. Results Here, we analyzed the gene duplications, interactions, and expression patterns of TIR1/AFBs and AUX/IAAs to understand their underlying mechanisms of evolution. The ratios of TIR1/AFBs to AUX/IAAs range from 4:2 in Physcomitrium patens to 6:29 in Arabidopsis thaliana and 3:16 in Fragaria vesca. Whole-genome duplication (WGD) and tandem duplication have contributed to the expansion of the AUX/IAA gene family, but numerous TIR1/AFB gene duplicates were lost after WGD. We further analyzed the expression profiles of TIR1/AFBs and AUX/IAAs in different tissue parts of Physcomitrium patens, Selaginella moellendorffii, Arabidopsis thaliana and Fragaria vesca, and found that TIR1/AFBs and AUX/IAAs were highly expressed in all tissues in P. patens, S. moellendorffii. In A. thaliana and F. vesca, TIR1/AFBs maintained the same expression pattern as the ancient plants with high expression in all tissue parts, while AUX/IAAs appeared tissue-specific expression. In F. vesca, 11 AUX/IAAs interacted with TIR1/AFBs with different interaction strengths, and the functional specificity of AUX/IAAs was related to their ability to bind TIR1/AFBs, thus promoting the development of specific higher plant organs. Verification of the interactions among TIR1/AFBs and AUX/IAAs in Marchantia polymorpha and F. vesca also showed that the regulation of AUX/IAA members by TIR1/AFBs became more refined over the course of plant evolution. Conclusions Our results indicate that specific interactions and specific gene expression patterns both contributed to the functional diversification of TIR1/AFBs and AUX/IAAs.
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spelling doaj.art-9162561810994e27a80cbf47dbf50c812023-05-21T11:12:32ZengBMCBMC Plant Biology1471-22292023-05-0123111010.1186/s12870-023-04253-4Different evolutionary patterns of TIR1/AFBs and AUX/IAAs and their implications for the morphogenesis of land plantsLiyao Su0Tian Zhang1Bin Yang2Tianyu Dong3Xiaoyu Liu4Yibo Bai5Hui Liu6Jingsong Xiong7Yan Zhong8Zong-Ming (Max) Cheng9State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Horticulture, Nanjing Agricultural UniversityState Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Horticulture, Nanjing Agricultural UniversityState Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Horticulture, Nanjing Agricultural UniversityState Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Horticulture, Nanjing Agricultural UniversityState Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Horticulture, Nanjing Agricultural UniversityState Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Horticulture, Nanjing Agricultural UniversityState Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Horticulture, Nanjing Agricultural UniversityState Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Horticulture, Nanjing Agricultural UniversityState Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Horticulture, Nanjing Agricultural UniversityState Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Horticulture, Nanjing Agricultural UniversityAbstract Background The plant hormone auxin is widely involved in plant growth, development, and morphogenesis, and the TIR1/AFB and AUX/IAA proteins are closely linked to rapid auxin response and signal transmission. However, their evolutionary history, historical patterns of expansion and contraction, and changes in interaction relationships are still unknown. Results Here, we analyzed the gene duplications, interactions, and expression patterns of TIR1/AFBs and AUX/IAAs to understand their underlying mechanisms of evolution. The ratios of TIR1/AFBs to AUX/IAAs range from 4:2 in Physcomitrium patens to 6:29 in Arabidopsis thaliana and 3:16 in Fragaria vesca. Whole-genome duplication (WGD) and tandem duplication have contributed to the expansion of the AUX/IAA gene family, but numerous TIR1/AFB gene duplicates were lost after WGD. We further analyzed the expression profiles of TIR1/AFBs and AUX/IAAs in different tissue parts of Physcomitrium patens, Selaginella moellendorffii, Arabidopsis thaliana and Fragaria vesca, and found that TIR1/AFBs and AUX/IAAs were highly expressed in all tissues in P. patens, S. moellendorffii. In A. thaliana and F. vesca, TIR1/AFBs maintained the same expression pattern as the ancient plants with high expression in all tissue parts, while AUX/IAAs appeared tissue-specific expression. In F. vesca, 11 AUX/IAAs interacted with TIR1/AFBs with different interaction strengths, and the functional specificity of AUX/IAAs was related to their ability to bind TIR1/AFBs, thus promoting the development of specific higher plant organs. Verification of the interactions among TIR1/AFBs and AUX/IAAs in Marchantia polymorpha and F. vesca also showed that the regulation of AUX/IAA members by TIR1/AFBs became more refined over the course of plant evolution. Conclusions Our results indicate that specific interactions and specific gene expression patterns both contributed to the functional diversification of TIR1/AFBs and AUX/IAAs.https://doi.org/10.1186/s12870-023-04253-4AuxinTIR1/AFBAUX/IAAInteractions patternGene retention and duplicationFunctional differentiation
spellingShingle Liyao Su
Tian Zhang
Bin Yang
Tianyu Dong
Xiaoyu Liu
Yibo Bai
Hui Liu
Jingsong Xiong
Yan Zhong
Zong-Ming (Max) Cheng
Different evolutionary patterns of TIR1/AFBs and AUX/IAAs and their implications for the morphogenesis of land plants
BMC Plant Biology
Auxin
TIR1/AFB
AUX/IAA
Interactions pattern
Gene retention and duplication
Functional differentiation
title Different evolutionary patterns of TIR1/AFBs and AUX/IAAs and their implications for the morphogenesis of land plants
title_full Different evolutionary patterns of TIR1/AFBs and AUX/IAAs and their implications for the morphogenesis of land plants
title_fullStr Different evolutionary patterns of TIR1/AFBs and AUX/IAAs and their implications for the morphogenesis of land plants
title_full_unstemmed Different evolutionary patterns of TIR1/AFBs and AUX/IAAs and their implications for the morphogenesis of land plants
title_short Different evolutionary patterns of TIR1/AFBs and AUX/IAAs and their implications for the morphogenesis of land plants
title_sort different evolutionary patterns of tir1 afbs and aux iaas and their implications for the morphogenesis of land plants
topic Auxin
TIR1/AFB
AUX/IAA
Interactions pattern
Gene retention and duplication
Functional differentiation
url https://doi.org/10.1186/s12870-023-04253-4
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