Deep transcriptomic study reveals the role of cell wall biosynthesis and organization networks in the developing shell of peanut pod

Abstract Background Peanut (Arachis hypogaea L.) belongs to an exceptional group of legume plants, wherein the flowers are produced aerially, but the pods develop under the ground. In such a unique environment, the pod’s outer shell plays a vital role as a barrier against mechanical damage and soilb...

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Autores principales:	Kapil Gupta, Shubhra Gupta, Adi Faigenboim-Doron, Abhinandan Surgonda Patil, Yael Levy, Scott Cohen Carrus, Ran Hovav
Formato:	article
Lenguaje:	EN
Publicado:	BMC 2021
Materias:	Cellulose synthases Cell Wall Pod wart Peanut Shell development Transcriptome Botany QK1-989
Acceso en línea:	https://doaj.org/article/38dee03f6b8c4c8b985f28b5ff61129b
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spelling	oai:doaj.org-article:38dee03f6b8c4c8b985f28b5ff61129b2021-11-07T12:09:14ZDeep transcriptomic study reveals the role of cell wall biosynthesis and organization networks in the developing shell of peanut pod10.1186/s12870-021-03290-11471-2229https://doaj.org/article/38dee03f6b8c4c8b985f28b5ff61129b2021-11-01T00:00:00Zhttps://doi.org/10.1186/s12870-021-03290-1https://doaj.org/toc/1471-2229Abstract Background Peanut (Arachis hypogaea L.) belongs to an exceptional group of legume plants, wherein the flowers are produced aerially, but the pods develop under the ground. In such a unique environment, the pod’s outer shell plays a vital role as a barrier against mechanical damage and soilborne pathogens. Recent studies have reported the uniqueness and importance of gene expression patterns that accompany peanut pods’ biogenesis. These studies focused on biogenesis and pod development during the early stages, but the late developmental stages and disease resistance aspects still have gaps. To extend this information, we analyzed the transcriptome generated from four pod developmental stages of two genotypes, Hanoch (Virginia-type) and IGC53 (Peruvian-type), which differs significantly in their pod shell characteristics and pathogen resistance. Results The transcriptome study revealed a significant reprogramming of the number and nature of differentially expressed (DE) genes during shell development. Generally, the numbers of DE genes were higher in IGC53 than in Hanoch, and the R5-R6 transition was the most dynamic in terms of transcriptomic changes. Genes related to cell wall biosynthesis, modification and transcription factors (TFs) dominated these changes therefore, we focused on their differential, temporal and spatial expression patterns. Analysis of the cellulose synthase superfamily identified specific Cellulose synthase (CesAs) and Cellulose synthase-like (Csl) genes and their coordinated interplay with other cell wall-related genes during the peanut shell development was demonstrated. TFs were also identified as being involved in the shell development process, and their pattern of expression differed in the two peanut genotypes. The shell component analysis showed that overall crude fiber, cellulose, lignin, hemicelluloses and dry matter increased with shell development, whereas K, N, protein, and ash content decreased. Genotype IGC53 contained a higher level of crude fiber, cellulose, NDF, ADF, K, ash, and dry matter percentage, while Hanoch had higher protein and nitrogen content. Conclusions The comparative transcriptome analysis identified differentially expressed genes, enriched processes, and molecular processes like cell wall biosynthesis/modifications, carbohydrate metabolic process, signaling, transcription factors, transport, stress, and lignin biosynthesis during the peanut shell development between two contrasting genotypes. TFs and other genes like chitinases were also enriched in peanut shells known for pathogen resistance against soilborne major pathogens causing pod wart disease and pod damages. This study will shed new light on the biological processes involved with underground pod development in an important legume crop.Kapil GuptaShubhra GuptaAdi Faigenboim-DoronAbhinandan Surgonda PatilYael LevyScott Cohen CarrusRan HovavBMCarticleCellulose synthasesCell WallPod wartPeanutShell developmentTranscriptomeBotanyQK1-989ENBMC Plant Biology, Vol 21, Iss 1, Pp 1-17 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Cellulose synthases Cell Wall Pod wart Peanut Shell development Transcriptome Botany QK1-989
spellingShingle	Cellulose synthases Cell Wall Pod wart Peanut Shell development Transcriptome Botany QK1-989 Kapil Gupta Shubhra Gupta Adi Faigenboim-Doron Abhinandan Surgonda Patil Yael Levy Scott Cohen Carrus Ran Hovav Deep transcriptomic study reveals the role of cell wall biosynthesis and organization networks in the developing shell of peanut pod
description	Abstract Background Peanut (Arachis hypogaea L.) belongs to an exceptional group of legume plants, wherein the flowers are produced aerially, but the pods develop under the ground. In such a unique environment, the pod’s outer shell plays a vital role as a barrier against mechanical damage and soilborne pathogens. Recent studies have reported the uniqueness and importance of gene expression patterns that accompany peanut pods’ biogenesis. These studies focused on biogenesis and pod development during the early stages, but the late developmental stages and disease resistance aspects still have gaps. To extend this information, we analyzed the transcriptome generated from four pod developmental stages of two genotypes, Hanoch (Virginia-type) and IGC53 (Peruvian-type), which differs significantly in their pod shell characteristics and pathogen resistance. Results The transcriptome study revealed a significant reprogramming of the number and nature of differentially expressed (DE) genes during shell development. Generally, the numbers of DE genes were higher in IGC53 than in Hanoch, and the R5-R6 transition was the most dynamic in terms of transcriptomic changes. Genes related to cell wall biosynthesis, modification and transcription factors (TFs) dominated these changes therefore, we focused on their differential, temporal and spatial expression patterns. Analysis of the cellulose synthase superfamily identified specific Cellulose synthase (CesAs) and Cellulose synthase-like (Csl) genes and their coordinated interplay with other cell wall-related genes during the peanut shell development was demonstrated. TFs were also identified as being involved in the shell development process, and their pattern of expression differed in the two peanut genotypes. The shell component analysis showed that overall crude fiber, cellulose, lignin, hemicelluloses and dry matter increased with shell development, whereas K, N, protein, and ash content decreased. Genotype IGC53 contained a higher level of crude fiber, cellulose, NDF, ADF, K, ash, and dry matter percentage, while Hanoch had higher protein and nitrogen content. Conclusions The comparative transcriptome analysis identified differentially expressed genes, enriched processes, and molecular processes like cell wall biosynthesis/modifications, carbohydrate metabolic process, signaling, transcription factors, transport, stress, and lignin biosynthesis during the peanut shell development between two contrasting genotypes. TFs and other genes like chitinases were also enriched in peanut shells known for pathogen resistance against soilborne major pathogens causing pod wart disease and pod damages. This study will shed new light on the biological processes involved with underground pod development in an important legume crop.
format	article
author	Kapil Gupta Shubhra Gupta Adi Faigenboim-Doron Abhinandan Surgonda Patil Yael Levy Scott Cohen Carrus Ran Hovav
author_facet	Kapil Gupta Shubhra Gupta Adi Faigenboim-Doron Abhinandan Surgonda Patil Yael Levy Scott Cohen Carrus Ran Hovav
author_sort	Kapil Gupta
title	Deep transcriptomic study reveals the role of cell wall biosynthesis and organization networks in the developing shell of peanut pod
title_short	Deep transcriptomic study reveals the role of cell wall biosynthesis and organization networks in the developing shell of peanut pod
title_full	Deep transcriptomic study reveals the role of cell wall biosynthesis and organization networks in the developing shell of peanut pod
title_fullStr	Deep transcriptomic study reveals the role of cell wall biosynthesis and organization networks in the developing shell of peanut pod
title_full_unstemmed	Deep transcriptomic study reveals the role of cell wall biosynthesis and organization networks in the developing shell of peanut pod
title_sort	deep transcriptomic study reveals the role of cell wall biosynthesis and organization networks in the developing shell of peanut pod
publisher	BMC
publishDate	2021
url	https://doaj.org/article/38dee03f6b8c4c8b985f28b5ff61129b
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Deep transcriptomic study reveals the role of cell wall biosynthesis and organization networks in the developing shell of peanut pod

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