Cargando…

The regulatory landscape of early maize inflorescence development

BACKGROUND: The functional genome of agronomically important plant species remains largely unexplored, yet presents a virtually untapped resource for targeted crop improvement. Functional elements of regulatory DNA revealed through profiles of chromatin accessibility can be harnessed for fine-tuning...

Descripción completa

Detalles Bibliográficos
Autores principales: Parvathaneni, Rajiv K., Bertolini, Edoardo, Shamimuzzaman, Md, Vera, Daniel L., Lung, Pei-Yau, Rice, Brian R., Zhang, Jinfeng, Brown, Patrick J., Lipka, Alexander E., Bass, Hank W., Eveland, Andrea L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7336428/
https://www.ncbi.nlm.nih.gov/pubmed/32631399
http://dx.doi.org/10.1186/s13059-020-02070-8
_version_ 1783554317127516160
author Parvathaneni, Rajiv K.
Bertolini, Edoardo
Shamimuzzaman, Md
Vera, Daniel L.
Lung, Pei-Yau
Rice, Brian R.
Zhang, Jinfeng
Brown, Patrick J.
Lipka, Alexander E.
Bass, Hank W.
Eveland, Andrea L.
author_facet Parvathaneni, Rajiv K.
Bertolini, Edoardo
Shamimuzzaman, Md
Vera, Daniel L.
Lung, Pei-Yau
Rice, Brian R.
Zhang, Jinfeng
Brown, Patrick J.
Lipka, Alexander E.
Bass, Hank W.
Eveland, Andrea L.
author_sort Parvathaneni, Rajiv K.
collection PubMed
description BACKGROUND: The functional genome of agronomically important plant species remains largely unexplored, yet presents a virtually untapped resource for targeted crop improvement. Functional elements of regulatory DNA revealed through profiles of chromatin accessibility can be harnessed for fine-tuning gene expression to optimal phenotypes in specific environments. RESULT: Here, we investigate the non-coding regulatory space in the maize (Zea mays) genome during early reproductive development of pollen- and grain-bearing inflorescences. Using an assay for differential sensitivity of chromatin to micrococcal nuclease (MNase) digestion, we profile accessible chromatin and nucleosome occupancy in these largely undifferentiated tissues and classify at least 1.6% of the genome as accessible, with the majority of MNase hypersensitive sites marking proximal promoters, but also 3′ ends of maize genes. This approach maps regulatory elements to footprint-level resolution. Integration of complementary transcriptome profiles and transcription factor occupancy data are used to annotate regulatory factors, such as combinatorial transcription factor binding motifs and long non-coding RNAs, that potentially contribute to organogenesis, including tissue-specific regulation between male and female inflorescence structures. Finally, genome-wide association studies for inflorescence architecture traits based solely on functional regions delineated by MNase hypersensitivity reveals new SNP-trait associations in known regulators of inflorescence development as well as new candidates. CONCLUSIONS: These analyses provide a comprehensive look into the cis-regulatory landscape during inflorescence differentiation in a major cereal crop, which ultimately shapes architecture and influences yield potential.
format Online
Article
Text
id pubmed-7336428
institution National Center for Biotechnology Information
language English
publishDate 2020
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-73364282020-07-07 The regulatory landscape of early maize inflorescence development Parvathaneni, Rajiv K. Bertolini, Edoardo Shamimuzzaman, Md Vera, Daniel L. Lung, Pei-Yau Rice, Brian R. Zhang, Jinfeng Brown, Patrick J. Lipka, Alexander E. Bass, Hank W. Eveland, Andrea L. Genome Biol Research BACKGROUND: The functional genome of agronomically important plant species remains largely unexplored, yet presents a virtually untapped resource for targeted crop improvement. Functional elements of regulatory DNA revealed through profiles of chromatin accessibility can be harnessed for fine-tuning gene expression to optimal phenotypes in specific environments. RESULT: Here, we investigate the non-coding regulatory space in the maize (Zea mays) genome during early reproductive development of pollen- and grain-bearing inflorescences. Using an assay for differential sensitivity of chromatin to micrococcal nuclease (MNase) digestion, we profile accessible chromatin and nucleosome occupancy in these largely undifferentiated tissues and classify at least 1.6% of the genome as accessible, with the majority of MNase hypersensitive sites marking proximal promoters, but also 3′ ends of maize genes. This approach maps regulatory elements to footprint-level resolution. Integration of complementary transcriptome profiles and transcription factor occupancy data are used to annotate regulatory factors, such as combinatorial transcription factor binding motifs and long non-coding RNAs, that potentially contribute to organogenesis, including tissue-specific regulation between male and female inflorescence structures. Finally, genome-wide association studies for inflorescence architecture traits based solely on functional regions delineated by MNase hypersensitivity reveals new SNP-trait associations in known regulators of inflorescence development as well as new candidates. CONCLUSIONS: These analyses provide a comprehensive look into the cis-regulatory landscape during inflorescence differentiation in a major cereal crop, which ultimately shapes architecture and influences yield potential. BioMed Central 2020-07-06 /pmc/articles/PMC7336428/ /pubmed/32631399 http://dx.doi.org/10.1186/s13059-020-02070-8 Text en © The Author(s) 2020 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Parvathaneni, Rajiv K.
Bertolini, Edoardo
Shamimuzzaman, Md
Vera, Daniel L.
Lung, Pei-Yau
Rice, Brian R.
Zhang, Jinfeng
Brown, Patrick J.
Lipka, Alexander E.
Bass, Hank W.
Eveland, Andrea L.
The regulatory landscape of early maize inflorescence development
title The regulatory landscape of early maize inflorescence development
title_full The regulatory landscape of early maize inflorescence development
title_fullStr The regulatory landscape of early maize inflorescence development
title_full_unstemmed The regulatory landscape of early maize inflorescence development
title_short The regulatory landscape of early maize inflorescence development
title_sort regulatory landscape of early maize inflorescence development
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7336428/
https://www.ncbi.nlm.nih.gov/pubmed/32631399
http://dx.doi.org/10.1186/s13059-020-02070-8
work_keys_str_mv AT parvathanenirajivk theregulatorylandscapeofearlymaizeinflorescencedevelopment
AT bertoliniedoardo theregulatorylandscapeofearlymaizeinflorescencedevelopment
AT shamimuzzamanmd theregulatorylandscapeofearlymaizeinflorescencedevelopment
AT veradaniell theregulatorylandscapeofearlymaizeinflorescencedevelopment
AT lungpeiyau theregulatorylandscapeofearlymaizeinflorescencedevelopment
AT ricebrianr theregulatorylandscapeofearlymaizeinflorescencedevelopment
AT zhangjinfeng theregulatorylandscapeofearlymaizeinflorescencedevelopment
AT brownpatrickj theregulatorylandscapeofearlymaizeinflorescencedevelopment
AT lipkaalexandere theregulatorylandscapeofearlymaizeinflorescencedevelopment
AT basshankw theregulatorylandscapeofearlymaizeinflorescencedevelopment
AT evelandandreal theregulatorylandscapeofearlymaizeinflorescencedevelopment
AT parvathanenirajivk regulatorylandscapeofearlymaizeinflorescencedevelopment
AT bertoliniedoardo regulatorylandscapeofearlymaizeinflorescencedevelopment
AT shamimuzzamanmd regulatorylandscapeofearlymaizeinflorescencedevelopment
AT veradaniell regulatorylandscapeofearlymaizeinflorescencedevelopment
AT lungpeiyau regulatorylandscapeofearlymaizeinflorescencedevelopment
AT ricebrianr regulatorylandscapeofearlymaizeinflorescencedevelopment
AT zhangjinfeng regulatorylandscapeofearlymaizeinflorescencedevelopment
AT brownpatrickj regulatorylandscapeofearlymaizeinflorescencedevelopment
AT lipkaalexandere regulatorylandscapeofearlymaizeinflorescencedevelopment
AT basshankw regulatorylandscapeofearlymaizeinflorescencedevelopment
AT evelandandreal regulatorylandscapeofearlymaizeinflorescencedevelopment