Integrated Analysis of Hi-C and RNA-Seq Reveals the Molecular Mechanism of Autopolyploid Growth Advantages in Pak Choi (Brassica rapa ssp. chinensis)

Polyploids generated by the replication of a single genome (autopolyploid) or synthesis of two or more distinct genomes (allopolyploid) usually show significant advantages over their diploid progenitors in biological characteristics, including growth and development, nutrient accumulation, and plant...

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Main Authors: Huiyuan Wu, Xiaoming Song, Shanwu Lyu, Yiming Ren, Tongkun Liu, Xilin Hou, Ying Li, Changwei Zhang
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-06-01
Series:Frontiers in Plant Science
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Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2022.905202/full
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author Huiyuan Wu
Xiaoming Song
Shanwu Lyu
Yiming Ren
Tongkun Liu
Xilin Hou
Ying Li
Changwei Zhang
author_facet Huiyuan Wu
Xiaoming Song
Shanwu Lyu
Yiming Ren
Tongkun Liu
Xilin Hou
Ying Li
Changwei Zhang
author_sort Huiyuan Wu
collection DOAJ
description Polyploids generated by the replication of a single genome (autopolyploid) or synthesis of two or more distinct genomes (allopolyploid) usually show significant advantages over their diploid progenitors in biological characteristics, including growth and development, nutrient accumulation, and plant resistance. Whereas, the impacts of genomic replication on transcription regulation and chromatin structure in pak choi have not been explored fully. In this study, we observed the transcriptional and genomic structural alterations between diploid B. rapa (AA) and artificial autotetraploid B. rapa (AAAA) using RNA-seq and Hi-C. RNA-seq revealed 1,786 differentially expressed genes (DEGs) between the diploids and autotetraploids, including 717 down-regulated and 1,069 up-regulated genes in autotetraploids. Of all the 1,786 DEGs, 23 DEGs (10 down-regulated DEGs in autotetraploids) were involved in Compartment A-B shifts, while 28 DEGs (20 up-regulated DEGs in autotetraploids) participated in Compartment B-A shifts. Moreover, there were 15 DEGs in activated topologically associating domains (TADs) (9 up-regulated DEGs in diploids) and 80 DEGs in repressed TADs (49 down-regulated DEGs in diploids). Subsequently, eight DEGs with genomic structural variants were selected as potential candidate genes, including four DEGs involved in photosynthesis (BraA01003143, BraA09002798, BraA04002224, and BraA08000594), three DEGs related to chloroplast (BraA05002974, BraA05001662, and BraA04001148), and one DEG associated with disease resistance (BraA09004451), which all showed high expression in autotetraploids. Overall, our results demonstrated that integrative RNA-seq and Hi-C analysis can identify related genes to phenotypic traits and also provided new insights into the molecular mechanism of the growth advantage of polyploids.
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spelling doaj.art-9a1f3a5cedd8451590121c5c8eb6ca942022-12-22T03:32:42ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-06-011310.3389/fpls.2022.905202905202Integrated Analysis of Hi-C and RNA-Seq Reveals the Molecular Mechanism of Autopolyploid Growth Advantages in Pak Choi (Brassica rapa ssp. chinensis)Huiyuan Wu0Xiaoming Song1Shanwu Lyu2Yiming Ren3Tongkun Liu4Xilin Hou5Ying Li6Changwei Zhang7State Key Laboratory of Crop Genetics and Germplasm Enhancement, Key Laboratory of Biology and Germplasm Enhancement of Horticultural Crops in East China, Ministry of Agriculture, Nanjing Agricultural University, Nanjing, ChinaCenter for Genomics and Bio-Computing, School of Life Sciences, North China University of Science and Technology, Tangshan, ChinaState Key Laboratory of Crop Genetics and Germplasm Enhancement, Key Laboratory of Biology and Germplasm Enhancement of Horticultural Crops in East China, Ministry of Agriculture, Nanjing Agricultural University, Nanjing, ChinaState Key Laboratory of Crop Genetics and Germplasm Enhancement, Key Laboratory of Biology and Germplasm Enhancement of Horticultural Crops in East China, Ministry of Agriculture, Nanjing Agricultural University, Nanjing, ChinaState Key Laboratory of Crop Genetics and Germplasm Enhancement, Key Laboratory of Biology and Germplasm Enhancement of Horticultural Crops in East China, Ministry of Agriculture, Nanjing Agricultural University, Nanjing, ChinaState Key Laboratory of Crop Genetics and Germplasm Enhancement, Key Laboratory of Biology and Germplasm Enhancement of Horticultural Crops in East China, Ministry of Agriculture, Nanjing Agricultural University, Nanjing, ChinaState Key Laboratory of Crop Genetics and Germplasm Enhancement, Key Laboratory of Biology and Germplasm Enhancement of Horticultural Crops in East China, Ministry of Agriculture, Nanjing Agricultural University, Nanjing, ChinaState Key Laboratory of Crop Genetics and Germplasm Enhancement, Key Laboratory of Biology and Germplasm Enhancement of Horticultural Crops in East China, Ministry of Agriculture, Nanjing Agricultural University, Nanjing, ChinaPolyploids generated by the replication of a single genome (autopolyploid) or synthesis of two or more distinct genomes (allopolyploid) usually show significant advantages over their diploid progenitors in biological characteristics, including growth and development, nutrient accumulation, and plant resistance. Whereas, the impacts of genomic replication on transcription regulation and chromatin structure in pak choi have not been explored fully. In this study, we observed the transcriptional and genomic structural alterations between diploid B. rapa (AA) and artificial autotetraploid B. rapa (AAAA) using RNA-seq and Hi-C. RNA-seq revealed 1,786 differentially expressed genes (DEGs) between the diploids and autotetraploids, including 717 down-regulated and 1,069 up-regulated genes in autotetraploids. Of all the 1,786 DEGs, 23 DEGs (10 down-regulated DEGs in autotetraploids) were involved in Compartment A-B shifts, while 28 DEGs (20 up-regulated DEGs in autotetraploids) participated in Compartment B-A shifts. Moreover, there were 15 DEGs in activated topologically associating domains (TADs) (9 up-regulated DEGs in diploids) and 80 DEGs in repressed TADs (49 down-regulated DEGs in diploids). Subsequently, eight DEGs with genomic structural variants were selected as potential candidate genes, including four DEGs involved in photosynthesis (BraA01003143, BraA09002798, BraA04002224, and BraA08000594), three DEGs related to chloroplast (BraA05002974, BraA05001662, and BraA04001148), and one DEG associated with disease resistance (BraA09004451), which all showed high expression in autotetraploids. Overall, our results demonstrated that integrative RNA-seq and Hi-C analysis can identify related genes to phenotypic traits and also provided new insights into the molecular mechanism of the growth advantage of polyploids.https://www.frontiersin.org/articles/10.3389/fpls.2022.905202/fullRNA-seqHi-CA/B compartmentTADsautopolyploidgrowth advantage
spellingShingle Huiyuan Wu
Xiaoming Song
Shanwu Lyu
Yiming Ren
Tongkun Liu
Xilin Hou
Ying Li
Changwei Zhang
Integrated Analysis of Hi-C and RNA-Seq Reveals the Molecular Mechanism of Autopolyploid Growth Advantages in Pak Choi (Brassica rapa ssp. chinensis)
Frontiers in Plant Science
RNA-seq
Hi-C
A/B compartment
TADs
autopolyploid
growth advantage
title Integrated Analysis of Hi-C and RNA-Seq Reveals the Molecular Mechanism of Autopolyploid Growth Advantages in Pak Choi (Brassica rapa ssp. chinensis)
title_full Integrated Analysis of Hi-C and RNA-Seq Reveals the Molecular Mechanism of Autopolyploid Growth Advantages in Pak Choi (Brassica rapa ssp. chinensis)
title_fullStr Integrated Analysis of Hi-C and RNA-Seq Reveals the Molecular Mechanism of Autopolyploid Growth Advantages in Pak Choi (Brassica rapa ssp. chinensis)
title_full_unstemmed Integrated Analysis of Hi-C and RNA-Seq Reveals the Molecular Mechanism of Autopolyploid Growth Advantages in Pak Choi (Brassica rapa ssp. chinensis)
title_short Integrated Analysis of Hi-C and RNA-Seq Reveals the Molecular Mechanism of Autopolyploid Growth Advantages in Pak Choi (Brassica rapa ssp. chinensis)
title_sort integrated analysis of hi c and rna seq reveals the molecular mechanism of autopolyploid growth advantages in pak choi brassica rapa ssp chinensis
topic RNA-seq
Hi-C
A/B compartment
TADs
autopolyploid
growth advantage
url https://www.frontiersin.org/articles/10.3389/fpls.2022.905202/full
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