skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Transcriptome and phenotyping analyses support a role for chloroplast sigma factor 2 in red‐light‐dependent regulation of growth, stress, and photosynthesis

Journal Article · · Plant Direct
DOI:https://doi.org/10.1002/pld3.43· OSTI ID:1423167
 [1];  [1];  [2];  [3];  [4]
  1. Department of Energy – Plant Research Laboratory Michigan State University East Lansing MI USA
  2. Department of Energy – Plant Research Laboratory Michigan State University East Lansing MI USA, Department of Biochemistry and Molecular Biology Michigan State University East Lansing MI USA
  3. UK Medical Center MN 150 University of Kentucky College of Medicine Lexington KY USA
  4. Department of Energy – Plant Research Laboratory Michigan State University East Lansing MI USA, Department of Biochemistry and Molecular Biology Michigan State University East Lansing MI USA, Department of Microbiology &, Molecular Genetics Michigan State University East Lansing MI USA

Abstract Sigma factor ( SIG ) proteins contribute to promoter specificity of the plastid‐encoded RNA polymerase during chloroplast genome transcription. All six members of the SIG family, that is, SIG 1– SIG 6, are nuclear‐encoded proteins targeted to chloroplasts. Sigma factor 2 ( SIG 2) is a phytochrome‐regulated protein important for stoichiometric control of the expression of plastid‐ and nuclear‐encoded genes that impact plastid development and plant growth and development. Among SIG factors, SIG 2 is required not only for transcription of chloroplast genes (i.e., anterograde signaling), but also impacts nuclear‐encoded, photosynthesis‐related, and light signaling‐related genes (i.e., retrograde signaling) in response to plastid functional status. Although SIG 2 is involved in photomorphogenesis in Arabidopsis, the molecular bases for its role in light signaling that impacts photomorphogenesis and aspects of photosynthesis have only recently begun to be investigated. Previously, we reported that SIG 2 is necessary for phytochrome‐mediated photomorphogenesis specifically under red (R) and far‐red light, thereby suggesting a link between phytochromes and nuclear‐encoded SIG 2 in light signaling. To explore transcriptional roles of SIG 2 in R‐dependent growth and development, we performed RNA sequencing analysis to compare gene expression in sig2‐2 mutant and Col‐0 wild‐type seedlings at two developmental stages (1‐ and 7‐day). We identified a subset of misregulated genes involved in growth, hormonal cross talk, stress responses, and photosynthesis. To investigate the functional relevance of these gene expression analyses, we performed several comparative phenotyping tests. In these analyses, strong sig2 mutants showed insensitivity to bioactive GA 3 , high intracellular levels of hydrogen peroxide (H 2 O 2 ) indicative of a stress response, and specific defects in photosynthesis, including elevated levels of cyclic electron flow ( CEF ) and nonphotochemical quenching ( NPQ ). We demonstrated that SIG 2 regulates a broader range of physiological responses at the molecular level than previously reported, with specific roles in red‐light‐mediated photomorphogenesis.

Sponsoring Organization:
USDOE
Grant/Contract Number:
DE‐FG02‐91ER2002
OSTI ID:
1423167
Alternate ID(s):
OSTI ID: 1423171
Journal Information:
Plant Direct, Journal Name: Plant Direct Vol. 2 Journal Issue: 2; ISSN 2475-4455
Publisher:
Wiley Blackwell (John Wiley & Sons)Copyright Statement
Country of Publication:
United Kingdom
Language:
English
Citation Metrics:
Cited by: 8 works
Citation information provided by
Web of Science

References (70)

Defects in the Expression of Chloroplast Proteins Leads to H2O2 Accumulation and Activation of Cyclic Electron Flow around Photosystem I journal January 2017
Gibberellins Repress Photomorphogenesis in Darkness journal February 2004
Phytochrome B Affects Responsiveness to Gibberellins in Arabidopsis journal September 1996
Phytochrome Regulation and Differential Expression of Gibberellin 3β-Hydroxylase Genes in Germinating Arabidopsis Seeds journal December 1998
Dynamic Environmental Photosynthetic Imaging Reveals Emergent Phenotypes journal June 2016
Activation of cyclic electron flow by hydrogen peroxide in vivo journal April 2015
Chloroplast development in Arabidopsis thaliana requires the nuclear-encoded transcription factor Sigma B journal November 2000
O-Glycosylated Cell Wall Proteins Are Essential in Root Hair Growth journal June 2011
Sigma factor-mediated plastid retrograde signals control nuclear gene expression journal November 2012
Plant Cell Walls: Figure 1. journal October 2010
The Importance of Energy Balance in Improving Photosynthetic Productivity journal November 2010
Cross Talk between H2O2 and Interacting Signal Molecules under Plant Stress Response journal April 2016
DELLA-mediated PIF degradation contributes to coordination of light and gibberellin signalling in Arabidopsis journal June 2016
An improved method, using saturating light pulses, for the determination of photosystem I quantum yield via P700+-absorbance changes at 830 nm journal January 1994
Coordinated regulation of Arabidopsis thaliana development by light and gibberellins journal January 2008
Detection of Spatial-Specific Phytochrome Responses Using Targeted Expression of Biliverdin Reductase in Arabidopsis journal October 2008
Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks journal March 2012
Methyl jasmonate, gibberellic acid, and auxin affect transcription and transcript accumulation of chloroplast genes in barley journal August 2011
Downstream effectors of light- and phytochrome-dependent regulation of hypocotyl elongation in Arabidopsis thaliana journal March 2013
Blue light specific and differential expression of a plastid σ factor, Sig5 in Arabidopsis thaliana journal March 2002
Gibberellin Biosynthesis in Arabidopsis journal February 2006
Cyclic photophosphorylation and electron transport journal April 1995
Quantification of cyclic electron flow around Photosystem I in spinach leaves during photosynthetic induction journal January 2007
The Dynamics of Photosynthesis journal December 2008
Integrating the proton circuit into photosynthesis: progress and challenges journal January 2005
The Regulation of Enzymes Involved in Chlorophyll Biosynthesis journal April 1996
Drought stress and reactive oxygen species: production, scavenging and signaling journal March 2008
The Multiple-Stress Responsive Plastid Sigma Factor, SIG5, Directs Activation of the psbD Blue Light-Responsive Promoter (BLRP) in Arabidopsis thaliana journal April 2004
Reactive Species and Antioxidants. Redox Biology Is a Fundamental Theme of Aerobic Life journal June 2006
PGR5 Is Involved in Cyclic Electron Flow around Photosystem I and Is Essential for Photoprotection in Arabidopsis journal August 2002
Cell Wall Heterogeneity in Root Development of Arabidopsis journal August 2016
Identification of a functional respiratory complex in chloroplasts through analysis of tobacco mutants containing disrupted plastid ndh genes journal February 1998
Modification of Distinct Aspects of Photomorphogenesis via Targeted Expression of Mammalian Biliverdin Reductase in Transgenic Arabidopsis Plants journal October 1999
Molecular cloning and functional expression of gibberellin 2- oxidases, multifunctional enzymes involved in gibberellin deactivation journal April 1999
Plasticity in light reactions of photosynthesis for energy production and photoprotection journal November 2004
Gibberellin metabolism: new insights revealed by the genes journal December 2000
An Arabidopsis Mutant with High Cyclic Electron Flow around Photosystem I ( hcef ) Involving the NADPH Dehydrogenase Complex journal January 2010
Phytochrome-dependent coordinate control of distinct aspects of nuclear and plastid gene expression during anterograde signaling and photomorphogenesis journal April 2014
Rewiring of jasmonate and phytochrome B signalling uncouples plant growth-defense tradeoffs journal August 2016
GO::TermFinder--open source software for accessing Gene Ontology information and finding significantly enriched Gene Ontology terms associated with a list of genes journal August 2004
Self-assembly of the plant cell wall requires an extensin scaffold journal February 2008
NAD(P)H Dehydrogenase-Dependent, Antimycin A-Sensitive Electron Donation to Plastoquinone in Tobacco Chloroplasts journal November 1998
Determining the limitations and regulation of photosynthetic energy transduction in leaves journal September 2007
New Subunits NDH-M, -N, and -O, Encoded by Nuclear Genes, Are Essential for Plastid Ndh Complex Functioning in Higher Plants journal December 2004
Extinction Coefficients of Chlorophyll a and b in N,N -Dimethylformamide and 80% Acetone journal February 1985
A nuclear-encoded sigma factor, Arabidopsis SIG6, recognizes sigma-70 type chloroplast promoters and regulates early chloroplast development in cotyledons: AtSIG6 general sigma factor in chloroplasts journal March 2005
Evidence That Putrescine Modulates the Higher Plant Photosynthetic Proton Circuit journal January 2012
Gibberellin Dose-Response Regulation of GA4 Gene Transcript Levels in Arabidopsis journal August 1998
Activity of photochemical reactions and accumulation of hydrogen peroxide in chloroplasts under stress conditions journal June 2008
Reconstitution of chlorophyllide formation by isolated etioplast membranes journal September 1978
Towards Characterization of the Chloroplast NAD(P)H Dehydrogenase Complex journal November 2009
Retrograde signaling in plants: from simple to complex scenarios journal January 2012
Structure and biogenesis of the chloroplast NAD(P)H dehydrogenase complex journal August 2011
16,17-Dihydro Gibberellin A 5 Competitively Inhibits a Recombinant Arabidopsis GA 3 β -Hydroxylase Encoded by the GA4 Gene journal June 2004
Redox Modulation of Cyclic Electron Flow around Photosystem I in C3 Plants journal November 2006
Hormonal Interactions in the Control of Arabidopsis Hypocotyl Elongation journal October 2000
Cyclic electron transfer in plant leaf journal July 2002
Plastidic RNA polymerase   factors in Arabidopsis journal January 1999
A Complex Containing PGRL1 and PGR5 Is Involved in the Switch between Linear and Cyclic Electron Flow in Arabidopsis journal January 2008
Recent advances in the study of chloroplast gene expression and its evolution journal January 2014
The Activity of the Chloroplastic Ndh Complex Is Regulated by Phosphorylation of the NDH-F Subunit journal April 2003
Phytochrome-induced SIG2 expression contributes to photoregulation of phytochrome signalling and photomorphogenesis in Arabidopsis thaliana journal September 2013
DELLAs Contribute to Plant Photomorphogenesis journal January 2007
Modulation of energy-dependent quenching of excitons in antennae of higher plants journal April 2004
Generation of Hydrogen Peroxide in Chloroplasts of Arabidopsis Overexpressing Glycolate Oxidase as an Inducible System to Study Oxidative Stress journal August 2008
The long-term responses of the photosynthetic proton circuit to drought journal March 2009
Efficient Operation of NAD(P)H Dehydrogenase Requires Supercomplex Formation with Photosystem I via Minor LHCI in Arabidopsis journal November 2009
Evidence for a general light-dependent negative control of NADPH-protochlorophyllide oxidoreductase in angiosperms journal December 1991
Next-Generation DNA Sequencing Methods journal September 2008
Role of the Extensin Superfamily in Primary Cell Wall Architecture journal March 2011

Related Subjects