Cargando…

Differential transcriptional networks associated with key phases of ingrowth wall construction in trans-differentiating epidermal transfer cells of Vicia faba cotyledons

BACKGROUND: Transfer cells are characterized by intricate ingrowth walls, comprising an uniform wall upon which wall ingrowths are deposited. The ingrowth wall forms a scaffold to support an amplified plasma membrane surface area enriched in membrane transporters that collectively confers transfer c...

Descripción completa

Detalles Bibliográficos
Autores principales: Zhang, Hui-Ming, Wheeler, Simon, Xia, Xue, Radchuk, Ruslana, Weber, Hans, Offler, Christina E, Patrick, John W
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4437447/
https://www.ncbi.nlm.nih.gov/pubmed/25887034
http://dx.doi.org/10.1186/s12870-015-0486-5
_version_ 1782372218201702400
author Zhang, Hui-Ming
Wheeler, Simon
Xia, Xue
Radchuk, Ruslana
Weber, Hans
Offler, Christina E
Patrick, John W
author_facet Zhang, Hui-Ming
Wheeler, Simon
Xia, Xue
Radchuk, Ruslana
Weber, Hans
Offler, Christina E
Patrick, John W
author_sort Zhang, Hui-Ming
collection PubMed
description BACKGROUND: Transfer cells are characterized by intricate ingrowth walls, comprising an uniform wall upon which wall ingrowths are deposited. The ingrowth wall forms a scaffold to support an amplified plasma membrane surface area enriched in membrane transporters that collectively confers transfer cells with an enhanced capacity for membrane transport at bottlenecks for apo-/symplasmic exchange of nutrients. However, the underlying molecular mechanisms regulating polarized construction of the ingrowth wall and membrane transporter profile are poorly understood. RESULTS: An RNAseq study of an inducible epidermal transfer cell system in cultured Vicia faba cotyledons identified transfer cell specific transcriptomes associated with uniform wall and wall ingrowth deposition. All functional groups of genes examined were expressed before and following transition to a transfer cell fate. What changed were the isoform profiles of expressed genes within functional groups. Genes encoding ethylene and Ca(2+) signal generation and transduction pathways were enriched during uniform wall construction. Auxin-and reactive oxygen species-related genes dominated during wall ingrowth formation and ABA genes were evenly expressed across ingrowth wall construction. Expression of genes encoding kinesins, formins and villins was consistent with reorganization of cytoskeletal components. Uniform wall and wall ingrowth specific expression of exocyst complex components and SNAREs suggested specific patterns of exocytosis while dynamin mediated endocytotic activity was consistent with establishing wall ingrowth loci. Key regulatory genes of biosynthetic pathways for sphingolipids and sterols were expressed across ingrowth wall construction. Transfer cell specific expression of cellulose synthases was absent. Rather xyloglucan, xylan and pectin biosynthetic genes were selectively expressed during uniform wall construction. More striking was expression of genes encoding enzymes for re-modelling/degradation of cellulose, xyloglucans, pectins and callose. Extensins dominated the cohort of expressed wall structural proteins and particularly so across wall ingrowth development. Ion transporters were selectively expressed throughout ingrowth wall development along with organic nitrogen transporters and a large group of ABC transporters. Sugar transporters were less represented. CONCLUSIONS: Pathways regulating signalling and intracellular organization were fine tuned whilst cell wall construction and membrane transporter profiles were altered substantially upon transiting to a transfer cell fate. Each phase of ingrowth wall construction was linked with unique cohorts of expressed genes. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12870-015-0486-5) contains supplementary material, which is available to authorized users.
format Online
Article
Text
id pubmed-4437447
institution National Center for Biotechnology Information
language English
publishDate 2015
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-44374472015-05-20 Differential transcriptional networks associated with key phases of ingrowth wall construction in trans-differentiating epidermal transfer cells of Vicia faba cotyledons Zhang, Hui-Ming Wheeler, Simon Xia, Xue Radchuk, Ruslana Weber, Hans Offler, Christina E Patrick, John W BMC Plant Biol Research Article BACKGROUND: Transfer cells are characterized by intricate ingrowth walls, comprising an uniform wall upon which wall ingrowths are deposited. The ingrowth wall forms a scaffold to support an amplified plasma membrane surface area enriched in membrane transporters that collectively confers transfer cells with an enhanced capacity for membrane transport at bottlenecks for apo-/symplasmic exchange of nutrients. However, the underlying molecular mechanisms regulating polarized construction of the ingrowth wall and membrane transporter profile are poorly understood. RESULTS: An RNAseq study of an inducible epidermal transfer cell system in cultured Vicia faba cotyledons identified transfer cell specific transcriptomes associated with uniform wall and wall ingrowth deposition. All functional groups of genes examined were expressed before and following transition to a transfer cell fate. What changed were the isoform profiles of expressed genes within functional groups. Genes encoding ethylene and Ca(2+) signal generation and transduction pathways were enriched during uniform wall construction. Auxin-and reactive oxygen species-related genes dominated during wall ingrowth formation and ABA genes were evenly expressed across ingrowth wall construction. Expression of genes encoding kinesins, formins and villins was consistent with reorganization of cytoskeletal components. Uniform wall and wall ingrowth specific expression of exocyst complex components and SNAREs suggested specific patterns of exocytosis while dynamin mediated endocytotic activity was consistent with establishing wall ingrowth loci. Key regulatory genes of biosynthetic pathways for sphingolipids and sterols were expressed across ingrowth wall construction. Transfer cell specific expression of cellulose synthases was absent. Rather xyloglucan, xylan and pectin biosynthetic genes were selectively expressed during uniform wall construction. More striking was expression of genes encoding enzymes for re-modelling/degradation of cellulose, xyloglucans, pectins and callose. Extensins dominated the cohort of expressed wall structural proteins and particularly so across wall ingrowth development. Ion transporters were selectively expressed throughout ingrowth wall development along with organic nitrogen transporters and a large group of ABC transporters. Sugar transporters were less represented. CONCLUSIONS: Pathways regulating signalling and intracellular organization were fine tuned whilst cell wall construction and membrane transporter profiles were altered substantially upon transiting to a transfer cell fate. Each phase of ingrowth wall construction was linked with unique cohorts of expressed genes. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12870-015-0486-5) contains supplementary material, which is available to authorized users. BioMed Central 2015-04-16 /pmc/articles/PMC4437447/ /pubmed/25887034 http://dx.doi.org/10.1186/s12870-015-0486-5 Text en © Zhang et al.; licensee BioMed Central. 2015 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0) which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. 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.
spellingShingle Research Article
Zhang, Hui-Ming
Wheeler, Simon
Xia, Xue
Radchuk, Ruslana
Weber, Hans
Offler, Christina E
Patrick, John W
Differential transcriptional networks associated with key phases of ingrowth wall construction in trans-differentiating epidermal transfer cells of Vicia faba cotyledons
title Differential transcriptional networks associated with key phases of ingrowth wall construction in trans-differentiating epidermal transfer cells of Vicia faba cotyledons
title_full Differential transcriptional networks associated with key phases of ingrowth wall construction in trans-differentiating epidermal transfer cells of Vicia faba cotyledons
title_fullStr Differential transcriptional networks associated with key phases of ingrowth wall construction in trans-differentiating epidermal transfer cells of Vicia faba cotyledons
title_full_unstemmed Differential transcriptional networks associated with key phases of ingrowth wall construction in trans-differentiating epidermal transfer cells of Vicia faba cotyledons
title_short Differential transcriptional networks associated with key phases of ingrowth wall construction in trans-differentiating epidermal transfer cells of Vicia faba cotyledons
title_sort differential transcriptional networks associated with key phases of ingrowth wall construction in trans-differentiating epidermal transfer cells of vicia faba cotyledons
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4437447/
https://www.ncbi.nlm.nih.gov/pubmed/25887034
http://dx.doi.org/10.1186/s12870-015-0486-5
work_keys_str_mv AT zhanghuiming differentialtranscriptionalnetworksassociatedwithkeyphasesofingrowthwallconstructionintransdifferentiatingepidermaltransfercellsofviciafabacotyledons
AT wheelersimon differentialtranscriptionalnetworksassociatedwithkeyphasesofingrowthwallconstructionintransdifferentiatingepidermaltransfercellsofviciafabacotyledons
AT xiaxue differentialtranscriptionalnetworksassociatedwithkeyphasesofingrowthwallconstructionintransdifferentiatingepidermaltransfercellsofviciafabacotyledons
AT radchukruslana differentialtranscriptionalnetworksassociatedwithkeyphasesofingrowthwallconstructionintransdifferentiatingepidermaltransfercellsofviciafabacotyledons
AT weberhans differentialtranscriptionalnetworksassociatedwithkeyphasesofingrowthwallconstructionintransdifferentiatingepidermaltransfercellsofviciafabacotyledons
AT offlerchristinae differentialtranscriptionalnetworksassociatedwithkeyphasesofingrowthwallconstructionintransdifferentiatingepidermaltransfercellsofviciafabacotyledons
AT patrickjohnw differentialtranscriptionalnetworksassociatedwithkeyphasesofingrowthwallconstructionintransdifferentiatingepidermaltransfercellsofviciafabacotyledons