Extensive Transcriptome Changes During Natural Onset and Release of Vegetative Bud Dormancy in Populus.

Glenn T Howe,Henry D Priest,Palitha Dharmawardhana,Todd C Mockler,David P Horvath,Steven H Strauss

doi:10.3389/fpls.2015.00989

Abstract

To survive winter, many perennial plants become endodormant, a state of suspended growth maintained even in favorable growing environments. To understand vegetative bud endodormancy, we collected paradormant, endodormant, and ecodormant axillary buds from Populus trees growing under natural conditions. Of 44,441 Populus gene models analyzed using NimbleGen microarrays, we found that 1,362 (3.1%) were differentially expressed among the three dormancy states, and 429 (1.0%) were differentially expressed during only one of the two dormancy transitions (FDR p-value < 0.05). Of all differentially expressed genes, 69% were down-regulated from paradormancy to endodormancy, which was expected given the lower metabolic activity associated with endodormancy. Dormancy transitions were accompanied by changes in genes associated with DNA methylation (via RNA-directed DNA methylation) and histone modifications (via Polycomb Repressive Complex 2), confirming and extending knowledge of chromatin modifications as major features of dormancy transitions. Among the chromatin-associated genes, two genes similar to SPT (SUPPRESSOR OF TY) were strongly up-regulated during endodormancy. Transcription factor genes and gene sets that were atypically up-regulated during endodormancy include a gene that seems to encode a trihelix transcription factor and genes associated with proteins involved in responses to ethylene, cold, and other abiotic stresses. These latter transcription factors include ETHYLENE INSENSITIVE 3 (EIN3), ETHYLENE-RESPONSIVE ELEMENT BINDING PROTEIN (EBP), ETHYLENE RESPONSE FACTOR (ERF), ZINC FINGER PROTEIN 10 (ZAT10), ZAT12, and WRKY DNA-binding domain proteins. Analyses of phytohormone-associated genes suggest important changes in responses to ethylene, auxin, and brassinosteroids occur during endodormancy. We found weaker evidence for changes in genes associated with salicylic acid and jasmonic acid, and little evidence for important changes in genes associated with gibberellins, abscisic acid, and cytokinin. We identified 315 upstream sequence motifs associated with eight patterns of gene expression, including novel motifs and motifs associated with the circadian clock and responses to photoperiod, cold, dehydration, and ABA. Analogies between flowering and endodormancy suggest important roles for genes similar to SQUAMOSA-PROMOTER BINDING PROTEIN-LIKE (SPL), DORMANCY ASSOCIATED MADS-BOX (DAM), and SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1).

Highlights

Dormancy, the temporary suspension of growth (Lang et al, 1987), is a regulated process that controls plant growth, development, and architecture. Lang et al (1987) subdivided dormancy processes into three types: paradormancy, endodormancy, and ecodormancy
We collected axillary buds on five dates between August and March, and assigned these samples to three dormancy states or treatments based on cluster analysis of gene expression data
We found multiple genes associated with DNA methylation and histone modifications that were differentially expressed during the induction and release of endodormancy

Summary

Introduction

The temporary suspension of growth (Lang et al, 1987), is a regulated process that controls plant growth, development, and architecture. Lang et al (1987) subdivided dormancy processes into three types: paradormancy, endodormancy, and ecodormancy. The temporary suspension of growth (Lang et al, 1987), is a regulated process that controls plant growth, development, and architecture. Lang et al (1987) subdivided dormancy processes into three types: paradormancy, endodormancy, and ecodormancy. Paradormancy denotes the state in which meristem growth (e.g., in buds or seeds) is inhibited by signals from other plant organs. Endodormancy denotes the state in which meristem growth is inhibited by signals within the meristem itself. In plants adapted to cold climates, vegetative buds typically become endodormant in the fall and early winter, and prolonged periods of chilling (i.e., temperatures slightly above freezing) are needed before growth can resume, even under favorable environmental conditions. Even after the release of endodormancy, plants may remain ecodormant because of harsh environmental conditions such as cold or drought that are not conducive to cell division and elongation

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