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 shade-avoidance 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.

Highlights

  • Senescence is a genetically controlled program usually activated to degrade macromolecules and mobilize nutrients in an orderly manner from dying parts of the plant to growing parts (Lim et al, 2007)

  • Only 53% of the 827 senescence-induced genes identified by Buchanan-Wollaston et al (2005) were upregulated by 3-fold or more in leaves of whole plants held in the dark, and only 22% of the developmental senescence-enhanced mRNA transcripts identified by van der Graaff et al (2006) were increased by 3-fold or more in detached leaves held in the dark or in individual leaves induced to senesce by shading

  • Knockout of the F-box gene ORESARA9 (ORE9; Woo et al, 2001), overexpression of C-REPEAT/DRE BINDING FACTOR2 (CBF2) (Sharabi-Schwager et al, 2010), and a gain in function of ORESARA12-1/ARABIDOPSIS HISTIDINE KINASE3 (AHK3; Kim et al, 2006) all affect the timing of both senescence programs

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Summary

Introduction

Senescence is a genetically controlled program usually activated to degrade macromolecules and mobilize nutrients in an orderly manner from dying parts of the plant to growing parts (Lim et al, 2007). Some of the key regulators are themselves SAGs. For example, the transcription factors Arabidopsis NAC DOMAIN CONTAINING PROTEIN29/NAC-LIKE ACTIVATED BY AP3/PI (ANAC029/AtNAP; Guo and Gan, 2006) and ANAC092/ORE1/AtNAC2 (Kim et al, 2009) are both up-regulated during development- and dark-induced senescence and positively regulate the timing of both senescence programs. The transcription factors Arabidopsis NAC DOMAIN CONTAINING PROTEIN29/NAC-LIKE ACTIVATED BY AP3/PI (ANAC029/AtNAP; Guo and Gan, 2006) and ANAC092/ORE1/AtNAC2 (Kim et al, 2009) are both up-regulated during development- and dark-induced senescence and positively regulate the timing of both senescence programs These findings illustrate that significant cross talk exists between both senescence programs and that research in dark-detached systems can provide insights into the biology behind both senescence programs

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