Carbon Deprivation-Driven Transcriptome Reprogramming in Detached Developmentally Arresting Arabidopsis Inflorescences      

Abstract

Senescence is genetically controlled and activated in mature tissues during aging. However, immature plant tissues also display senescence-like symptoms when continuously exposed to adverse energy-depleting conditions. We used detached dark-held immature inflorescences of Arabidopsis (Arabidopsis thaliana) to understand the metabolic reprogramming occurring in immature tissues transitioning from rapid growth to precocious senescence. Macroscopic growth of the detached inflorescences rapidly ceased upon placement in water in the dark at 21°C. Inflorescences were completely degreened by 120 h of dark incubation and by 24 h had already lost 24% of their chlorophyll and 34% of their protein content. Comparative transcriptome profiling at 24 h revealed that inflorescence response at 24 h had a large carbon-deprivation component. Genes that positively regulate developmental senescence (ARABIDOPSIS NAC DOMAIN CONTAINING PROTEIN92) and shadeavoidance syndrome (PHYTOCHROME INTERACTING FACTOR4 [PIF4] and PIF5) were up-regulated within 24 h. Mutations in these genes delayed degreening of the inflorescences. Their up-regulation was suppressed in dark-held inflorescences by glucose treatment, which promoted macroscopic growth and development and inhibited degreening of the inflorescences. Detached inflorescences held in the dark for 4 d were still able to reinitiate development to produce siliques upon being brought out to the light, indicating that the transcriptional reprogramming at 24 h was adaptive and reversible. Our results suggest that the response of detached immature tissues to dark storage involves interactions between carbohydrate status sensing and light deprivation signaling and that the dark-adaptive response of the tissues appears to utilize some of the same key regulators as developmental senescence.

Early differential gene expression profiling of harvest-induced senescence in detached Arabidopsis plants

“…It was thought that AtCLH1 and AtCLH2 were indispensable for this reaction in Arabidopsis. However, in our study, AtCLH1 was downregulated in detached plants, which was consistent with different transcripts identified in the dark-detached inflorescences of Arabidopsis (Trivellini et al 2012). On the basis of Schenk et al (2007), single and double knockout lines of clh1 and clh2 are still capable of degrading chlorophyll during senescence, indicating that AtCLHs are not required for senescence-related chlorophyll degradation in Arabidopsis.…”

“…The downregulated genes were mainly involved in ribosome activities, metabolism, and photosynthesis, such as glycolysis/gluconeogenesis, purine metabolism, starch and sucrose metabolism, carbon fixation, and porphyrin and chlorophyll metabolism. These categories were greatly identical to those identified in the dark-detached inflorescences of Arabidopsis (Trivellini et al 2012). …”

“…Soluble proteins were extracted through the method of Trivellini et al (2012). 5 mg tissue was ground in liquid nitrogen and then 50 mL extraction buffer including 100 mM Tris-HCl, pH 7.6, 10 mM MgSO 4 , and 10 mM dithiothreitol was added.…”

Transcription Factor ATAF1 in Arabidopsis Promotes Senescence by Direct Regulation of Key Chloroplast Maintenance and Senescence Transcriptional Cascades

“…As shown by several laboratories independently, ORE1 is a key positive regulator of senescence in Arabidopsis, limiting the longevity of leaves, cotyledons, and inflorescences (Kim et al, 2009;Balazadeh et al, 2010a;Trivellini et al, 2012). In accordance with this, several SAGs have been identified to be under direct or indirect control of ORE1 (Balazadeh et al, 2010a;Breeze et al, 2011;Matallana-Ramirez et al, 2013;Rauf et al, 2013a), highlighting this NAC as one of the core control elements of the transcriptome underlying the senescence syndrome.…”

Spatial and temporal transcriptome changes occurring during flower opening and senescence of the ephemeral hibiscus flower,Hibiscus rosa-sinensis

“…darkness) in regulating plant senescence has been reported in a number of studies (Weaver and Amasino, 2001; Buchanan-Wollaston et al , 2005; van der Graaff et al , 2006). More recent research has now revealed how classic light signalling connects to senescence in two different Arabidopsis tissue systems: leaves (Song et al , 2014; Sakuraba et al , 2014) and inflorescences (Trivellini et al , 2012). …”