Four distinct types of dehydration stress memory genes in Arabidopsis thaliana

Abstract

BackgroundHow plants respond to dehydration stress has been extensively researched. However, how plants respond to multiple consecutive stresses is virtually unknown. Pre-exposure to various abiotic stresses (including dehydration) may alter plants’ subsequent responses by improving resistance to future exposures. These observations have led to the concept of ‘stress memory’ implying that during subsequent exposures plants provide responses that are different from those during their first encounter with the stress. Genes that provide altered responses in a subsequent stress define the ‘memory genes’ category; genes responding similarly to each stress form the ‘non-memory’ category.ResultsUsing a genome-wide RNA-Seq approach we determine the transcriptional responses of Arabidopsis plants that have experienced multiple exposures to dehydration stress and compare them with the transcriptional behavior of plants encountering the stress for the first time. The major contribution of this study is the revealed existence of four distinct, previously unknown, transcription memory response patterns of dehydration stress genes in A.thaliana. The biological relevance for each of the four memory types is considered in the context of four overlapping strategies employed by a plant to improve its stress tolerance and/or survival: 1) increased synthesis of protective, damage-repairing, and detoxifying functions; 2) coordinating photosynthesis and growth under repetitive stress; 3) re-adjusting osmotic and ionic equilibrium to maintain homeostasis; and 4) re-adjusting interactions between dehydration and other stress/hormone regulated pathways.ConclusionsThe results reveal the unknown, hitherto, existence of four distinct transcription memory response types in a plant and provide genome-wide characterization of memory and non-memory dehydration stress response genes in A.thaliana. The transcriptional responses during repeated exposures to stress are different from known responses occurring during a single exposure. GO analyses of encoded proteins suggested implications for the cellular/organismal protective, adaptive, and survival functions encoded by the memory genes. The results add a new dimension to our understanding of plants’ responses to dehydration stress and to current models for interactions between different signaling systems when adjusting to repeated spells of water deficits.

Rapid Recovery Gene Downregulation during Excess-Light Stress and Recovery in Arabidopsis

“…Building upon these criteria we observe six profiles (Supplemental Figure 11), including hyper, rapid, persistent (Figure 11), gain (e.g., AT1G21940), loss (e.g., AT3g03260), and inversion (e.g., AT1G66700; see Supplemental Data Set 4). Consistent with reports for dehydration stress in Arabidopsis (Ding et al, 2012b(Ding et al, , 2013, significant occurrences of hyperresponsiveness were identified; nevertheless, the response to the second stress was predominately the same as the response to the first stress (III versus I compared with XI versus IX). Of the 8800 transcripts responsive to the second stress exposure (XI versus X, padj < 0.05), 394 exhibited hyperinduction and 192 hyperrepression (Figures 11B and 11C; all stress memory transcripts are listed in Supplemental Data Set 14).…”

“…Four dehydration stress memory types were proposed (Ding et al, 2012b(Ding et al, , 2013Avramova, 2015). Building upon these criteria we observe six profiles (Supplemental Figure 11), including hyper, rapid, persistent (Figure 11), gain (e.g., AT1G21940), loss (e.g., AT3g03260), and inversion (e.g., AT1G66700; see Supplemental Data Set 4).…”

Photorespiration Is Crucial for Dynamic Response of Photosynthetic Metabolism and Stomatal Movement to Altered CO 2 Availability

“…Among the most downregulated genes shared between the strong mutants two transcription factors were detected (Table 2; HBI1 and BZIP61). The majority of these transcriptional regulators, RAP2.6, ABR1, AT1G10585, AT1G71520, and WRKY40, were characterized as being involved in the response to drought stress and ABA (Pandey et al, 2005;Chen et al, 2010;Zhu et al, 2010;Ding et al, 2013). In all strong mutants the transcripts of DIN11 and WRKY75 were induced, both of which are involved in starvation responses.…”

The Arabidopsis DNA Methylome Is Stable under Transgenerational Drought Stress

“…However, bona fide examples of transgenerational methylation changes leading to substantially altered plant behavior remain a rare observation (Pecinka et al, 2009;Becker et al, 2011;Jiang et al, 2014;Seymour et al, 2014;Crisp et al, 2016), with the majority of DNA methylome variation attributable to underlying genetic differences rather than being truly epigenetic (Eichten et al, 2013Schmitz et al, 2013;Li et al, 2014;Seymour et al, 2014;Dubin et al, 2015;Hagmann et al, 2015). Furthermore, there are a growing number of conflicting reports of short-term adaptation to abiotic stresses, including salt or drought stress, that occur independently of DNA methylation changes (Cayuela et al, 1996;Jakab et al, 2005;Rossel et al, 2007;Ding et al, 2012Ding et al, , 2013Ding et al, , 2014Gordon et al, 2013;Sani et al, 2013). This is in contrast to the potential for DNA methylationmediated transgenerational memory (Luo et al, 1996;Tricker et al, 2013;Herman and Sultan, 2016;Nosalewicz et al, 2016;Wibowo et al, 2016;Zheng et al, 2017).…”