A gene co-expression network predicts functional genes controlling the re-establishment of desiccation tolerance in germinated Arabidopsis thaliana seeds.

Maria Cecília D Costa,Harm Nijveen,Wilco Ligterink,Karima Righetti,Farzaneh Yazdanpanah,Henk W M Hilhorst,Julia Buitink

doi:10.1007/s00425-015-2283-7

Maria Cecília D Costa, Harm Nijveen + Show 5 more

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https://doi.org/10.1007/s00425-015-2283-7

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Abstract

Main conclusion During re-establishment of desiccation tolerance (DT), early events promote initial protection and growth arrest, while late events promote stress adaptation and contribute to survival in the dry state. Mature seeds of Arabidopsis thaliana are desiccation tolerant, but they lose desiccation tolerance (DT) while progressing to germination. Yet, there is a small developmental window during which DT can be rescued by treatment with abscisic acid (ABA). To gain temporal resolution and identify relevant genes in this process, data from a time series of microarrays were used to build a gene co-expression network. The network has two regions, namely early response (ER) and late response (LR). Genes in the ER region are related to biological processes, such as dormancy, acquisition of DT and drought, amplification of signals, growth arrest and induction of protection mechanisms (such as LEA proteins). Genes in the LR region lead to inhibition of photosynthesis and primary metabolism, promote adaptation to stress conditions and contribute to seed longevity. Phenotyping of 12 hubs in relation to re-establishment of DT with T-DNA insertion lines indicated a significant increase in the ability to re-establish DT compared with the wild-type in the lines cbsx4, at3g53040 and at4g25580, suggesting the operation of redundant and compensatory mechanisms. Moreover, we show that re-establishment of DT by polyethylene glycol and ABA occurs through partially overlapping mechanisms. Our data confirm that co-expression network analysis is a valid approach to examine data from time series of transcriptome analysis, as it provides promising insights into biologically relevant relations that help to generate new information about the roles of certain genes for DT.Electronic supplementary materialThe online version of this article (doi:10.1007/s00425-015-2283-7) contains supplementary material, which is available to authorized users.

Highlights

During seed development, orthodox seeds acquire the remarkable ability to tolerate desiccation
Incubation in PEG induces membrane changes, inhibits radicle growth, down-regulates genes related to energy metabolism and cell wall modification, up-regulates genes related to antioxidant activity, response to stress and seed storage, and induces synthesis of protective molecules, such as non-reducing sugars and certain proteins, such as late embryogenesis abundant (LEA) and heat shock proteins (HSPs) (Buitink et al 2003, 2006; Maia et al 2011)
Genes coding for abscisic acid (ABA) signal transduction elements and drought/stress-induced transcription factors (TFs) are up-regulated, leading to the hypothesis of a partial overlap of ABA-dependent and ABA-independent regulatory pathways involved in both drought and desiccation tolerance (DT) (Buitink et al 2003, 2006; Maia et al 2011)

Summary

Introduction

Orthodox seeds acquire the remarkable ability to tolerate desiccation This means that during development, as a part of the maturation phase, Planta (2015) 242:435–449 these seeds experience slow reduction of their water content to less than 5 % of their dry weight with little or no loss of viability (Ooms et al 1993). In this dry state, orthodox seeds can survive for years or centuries, which permit their storage and ensure better dispersal (Ramanjulu and Bartels 2002). Treatment of germinated seeds with ABA alone is able to re-establish DT (Maia et al 2014), the regulatory and mechanistic pathways activated via ABA remain to be elucidated

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