Light-responsive expression atlas reveals the effects of light quality and intensity in Kalanchoë fedtschenkoi, a plant with crassulacean acid metabolism

Abstract Background Crassulacean acid metabolism (CAM), a specialized mode of photosynthesis, enables plant adaptation to water-limited environments and improves photosynthetic efficiency via an inorganic carbon-concentrating mechanism. Kalanchoë fedtschenkoi is an obligate CAM model featuring a relatively small genome and easy stable transformation. However, the molecular responses to light quality and intensity in CAM plants remain understudied. Results Here we present a genome-wide expression atlas of K. fedtschenkoi plants grown under 12 h/12 h photoperiod with different light quality (blue, red, far-red, white light) and intensity (0, 150, 440, and 1,000 μmol m–2 s–1) based on RNA sequencing performed for mature leaf samples collected at dawn (2 h before the light period) and dusk (2 h before the dark period). An eFP web browser was created for easy access of the gene expression data. Based on the expression atlas, we constructed a light-responsive co-expression network to reveal the potential regulatory relationships in K. fedtschenkoi. Measurements of leaf titratable acidity, soluble sugar, and starch turnover provided metabolic indicators of the magnitude of CAM under the different light treatments and were used to provide biological context for the expression dataset. Furthermore, CAM-related subnetworks were highlighted to showcase genes relevant to CAM pathway, circadian clock, and stomatal movement. In comparison with white light, monochrome blue/red/far-red light treatments repressed the expression of several CAM-related genes at dusk, along with a major reduction in acid accumulation. Increasing light intensity from an intermediate level (440 μmol m−2 s−1) of white light to a high light treatment (1,000 μmol m–2 s–1) increased expression of several genes involved in dark CO2 fixation and malate transport at dawn, along with an increase in organic acid accumulation. Conclusions This study provides a useful genomics resource for investigating the molecular mechanism underlying the light regulation of physiology and metabolism in CAM plants. Our results support the hypothesis that both light intensity and light quality can modulate the CAM pathway through regulation of CAM-related genes in K. fedtschenkoi.

[1]  R. Varshney,et al.  The RNA-Seq-based high resolution gene expression atlas of chickpea (Cicer arietinum L.) reveals dynamic spatio-temporal changes associated with growth and development. , 2018, Plant, cell & environment.

[2]  N. Provart,et al.  The transcriptional landscape of polyploid wheat , 2018, Science.

[3]  Tetsuya Mori,et al.  Metabolic Reprogramming in Leaf Lettuce Grown Under Different Light Quality and Intensity Conditions Using Narrow-Band LEDs , 2018, Scientific Reports.

[4]  Deborah A. Weighill,et al.  The Kalanchoë genome provides insights into convergent evolution and building blocks of crassulacean acid metabolism , 2017, Nature Communications.

[5]  L. Roden,et al.  Plant circadian networks and responses to the environment. , 2017, Functional plant biology : FPB.

[6]  N. Provart,et al.  Expression atlas and comparative coexpression network analyses reveal important genes involved in the formation of lignified cell wall in Brachypodium distachyon. , 2017, The New phytologist.

[7]  R. Varshney,et al.  Gene expression atlas of pigeonpea and its application to gain insights into genes associated with pollen fertility implicated in seed formation , 2017, Journal of experimental botany.

[8]  Sheng-xin Chang,et al.  An RNA-Seq Analysis of Grape Plantlets Grown in vitro Reveals Different Responses to Blue, Green, Red LED Light, and White Fluorescent Light , 2017, Front. Plant Sci..

[9]  M. Logacheva,et al.  A high resolution map of the Arabidopsis thaliana developmental transcriptome based on RNA-seq profiling. , 2016, The Plant journal : for cell and molecular biology.

[10]  Xinyuan Hao,et al.  Transcriptomic analysis of the effects of three different light treatments on the biosynthesis of characteristic compounds in the tea plant by RNA-Seq , 2016, Tree Genetics & Genomes.

[11]  I. Kavakli,et al.  RNA-seq analysis of the transcriptional response to blue and red light in the extremophilic red alga, Cyanidioschyzon merolae , 2016, Functional & Integrative Genomics.

[12]  X. Deng,et al.  BBX21, an Arabidopsis B-box protein, directly activates HY5 and is targeted by COP1 for 26S proteasome-mediated degradation , 2016, Proceedings of the National Academy of Sciences.

[13]  J. Hartwell,et al.  Emerging model systems for functional genomics analysis of Crassulacean acid metabolism. , 2016, Current opinion in plant biology.

[14]  P. Más,et al.  MYB96 shapes the circadian gating of ABA signaling in Arabidopsis , 2016, Scientific Reports.

[15]  D. Weston,et al.  Climate-resilient agroforestry: physiological responses to climate change and engineering of crassulacean acid metabolism (CAM) as a mitigation strategy. , 2015, Plant, cell & environment.

[16]  Dawn H. Nagel,et al.  Genome-wide identification of CCA1 targets uncovers an expanded clock network in Arabidopsis , 2015, Proceedings of the National Academy of Sciences.

[17]  Junhui Wang,et al.  Transcriptome Analysis Reveals that Red and Blue Light Regulate Growth and Phytohormone Metabolism in Norway Spruce [Picea abies (L.) Karst.] , 2015, PloS one.

[18]  Karen Schlauch,et al.  A roadmap for research on crassulacean acid metabolism (CAM) to enhance sustainable food and bioenergy production in a hotter, drier world. , 2015, The New phytologist.

[19]  W. Huber,et al.  Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 , 2014, Genome Biology.

[20]  T. Zhao,et al.  CONSTANS-LIKE 7 (COL7) is involved in phytochrome B (phyB)-mediated light-quality regulation of auxin homeostasis. , 2014, Molecular plant.

[21]  L. Kozma-Bognár,et al.  The Arabidopsis ZINC FINGER PROTEIN3 Interferes with Abscisic Acid and Light Signaling in Seed Germination and Plant Development1[C][W][OPEN] , 2014, Plant Physiology.

[22]  A. Borland,et al.  Light quality modulates metabolic synchronization over the diel phases of crassulacean acid metabolism , 2014, Journal of experimental botany.

[23]  T. Tschaplinski,et al.  Engineering crassulacean acid metabolism to improve water-use efficiency. , 2014, Trends in plant science.

[24]  Wei Shi,et al.  featureCounts: an efficient general purpose program for assigning sequence reads to genomic features , 2013, Bioinform..

[25]  Cole Trapnell,et al.  TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions , 2013, Genome Biology.

[26]  Xiaoyin Liu,et al.  Effects of light intensity on the growth and leaf development of young tomato plants grown under a combination of red and blue light , 2013 .

[27]  Xuncheng Liu,et al.  PHYTOCHROME INTERACTING FACTOR3 Associates with the Histone Deacetylase HDA15 in Repression of Chlorophyll Biosynthesis and Photosynthesis in Etiolated Arabidopsis Seedlings[W][OA] , 2013, Plant Cell.

[28]  U. Lüttge,et al.  Independent fluctuations of malate and citrate in the CAM species Clusia hilariana Schltdl. under low light and high light in relation to photoprotection. , 2013, Journal of plant physiology.

[29]  L. Ponnala,et al.  Tissue- and Cell-Type Specific Transcriptome Profiling of Expanding Tomato Fruit Provides Insights into Metabolic and Regulatory Specialization and Cuticle Formation[W][OA] , 2011, Plant Cell.

[30]  Colin N. Dewey,et al.  RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome , 2011, BMC Bioinformatics.

[31]  Steve A. Kay,et al.  The ELF4-ELF3-LUX Complex Links the Circadian Clock to Diurnal Control of Hypocotyl Growth , 2011, Nature.

[32]  M. Shimizu,et al.  Sigma factor phosphorylation in the photosynthetic control of photosystem stoichiometry , 2010, Proceedings of the National Academy of Sciences.

[33]  Serban Nacu,et al.  Fast and SNP-tolerant detection of complex variants and splicing in short reads , 2010, Bioinform..

[34]  U. Lüttge,et al.  Adaptation of the obligate CAM plant Clusia alata to light stress: Metabolic responses. , 2009, Journal of plant physiology.

[35]  C. Kubota,et al.  Effects of supplemental light quality on growth and phytochemicals of baby leaf lettuce , 2009 .

[36]  M. Jones,et al.  REVEILLE1, a Myb-like transcription factor, integrates the circadian clock and auxin pathways , 2009, Proceedings of the National Academy of Sciences.

[37]  M. Yanovsky,et al.  Synergism of Red and Blue Light in the Control of Arabidopsis Gene Expression and Development , 2009, Current Biology.

[38]  J. Meurer,et al.  Arabidopsis mutants carrying chimeric sigma factor genes reveal regulatory determinants for plastid gene expression. , 2009, Plant & cell physiology.

[39]  E. Tobin,et al.  CIRCADIAN CLOCK ASSOCIATED1 and LATE ELONGATED HYPOCOTYL Function Synergistically in the Circadian Clock of Arabidopsis1[W][OA] , 2009, Plant Physiology.

[40]  S. Horvath,et al.  WGCNA: an R package for weighted correlation network analysis , 2008, BMC Bioinformatics.

[41]  Y. Onda,et al.  Light induction of Arabidopsis SIG1 and SIG5 transcripts in mature leaves: differential roles of cryptochrome 1 and cryptochrome 2 and dual function of SIG5 in the recognition of plastid promoters. , 2008, The Plant journal : for cell and molecular biology.

[42]  G. Weiller,et al.  A gene expression atlas of the model legume Medicago truncatula. , 2008, The Plant journal : for cell and molecular biology.

[43]  D. Galbraith,et al.  Diurnal and Circadian Rhythms in the Tomato Transcriptome and Their Modulation by Cryptochrome Photoreceptors , 2008, PloS one.

[44]  F. Gubler,et al.  Regulation of Dormancy in Barley by Blue Light and After-Ripening: Effects on Abscisic Acid and Gibberellin Metabolism1[W] , 2008, Plant Physiology.

[45]  N. Fukuda,et al.  Directional blue light irradiation triggers epidermal cell elongation of abaxial side resulting in inhibition of leaf epinasty in geranium under red light condition , 2008 .

[46]  Michael B. Stadler,et al.  MicroRNA-Mediated Regulation of Stomatal Development in Arabidopsis[W][OA] , 2007, The Plant Cell Online.

[47]  Hongya Gu,et al.  Constitutive expression of CIR1 (RVE2) affects several circadian-regulated processes and seed germination in Arabidopsis. , 2007, The Plant journal : for cell and molecular biology.

[48]  R. Emery,et al.  The interaction of light quality and irradiance with gibberellins, cytokinins and auxin in regulating growth of Helianthus annuus hypocotyls. , 2007, Plant, cell & environment.

[49]  Olavi Junttila,et al.  Effects of red, far-red and blue light in maintaining growth in latitudinal populations of Norway spruce (Picea abies). , 2006, Plant, cell & environment.

[50]  P. Quail,et al.  ELF4 is a phytochrome-regulated component of a negative-feedback loop involving the central oscillator components CCA1 and LHY. , 2005, The Plant journal : for cell and molecular biology.

[51]  Martin Kuiper,et al.  BiNGO: a Cytoscape plugin to assess overrepresentation of Gene Ontology categories in Biological Networks , 2005, Bioinform..

[52]  Jose L Pruneda-Paz,et al.  LUX ARRHYTHMO encodes a Myb domain protein essential for circadian rhythms. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[53]  S. Rhee,et al.  MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. , 2004, The Plant journal : for cell and molecular biology.

[54]  Chentao Lin,et al.  Cryptochrome structure and signal transduction. , 2003, Annual review of plant biology.

[55]  X. Xu,et al.  The Novel MYB Protein EARLY-PHYTOCHROME-RESPONSIVE1 Is a Component of a Slave Circadian Oscillator in Arabidopsis Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.014217. , 2003, The Plant Cell Online.

[56]  B. Pogson,et al.  Global Changes in Gene Expression in Response to High Light in Arabidopsis1,212 , 2002, Plant Physiology.

[57]  T. Grams,et al.  High light-induced switch from C(3)-photosynthesis to Crassulacean acid metabolism is mediated by UV-A/blue light. , 2002, Journal of experimental botany.

[58]  T. Shiina,et al.  Blue light specific and differential expression of a plastid σ factor, Sig5 in Arabidopsis thaliana , 2002, FEBS letters.

[59]  H. Griffiths,et al.  Crassulacean acid metabolism: plastic, fantastic. , 2002, Journal of experimental botany.

[60]  P. Quail,et al.  Phytochrome photosensory signalling networks , 2002, Nature Reviews Molecular Cell Biology.

[61]  J C Watson,et al.  The Phototropin Family of Photoreceptors , 2001, Plant Cell.

[62]  J. Zavala,et al.  Allocation of photoassimilates to biomass, resin and carbohydrates in Grindelia chiloensis as affected by light intensity , 2001 .

[63]  A. Borland,et al.  Crassulacean acid metabolism under severe light limitation: a matter of plasticity in the shadows? , 2011, Journal of experimental botany.

[64]  L. Ponnala,et al.  Tissue- and Cell-Type Specific Transcriptome Profiling of Expanding Tomato Fruit Provides Insights into Metabolic and Regulatory Specialization and Cuticle Formation , 2011 .

[65]  B. Tague,et al.  AtZFP1, encoding Arabidopsis thaliana C2H2 zinc-finger protein 1, is expressed downstream of photomorphogenic activation , 2004, Plant Molecular Biology.

[66]  Eberhard Schäfer,et al.  Phytochromes control photomorphogenesis by differentially regulated, interacting signaling pathways in higher plants. , 2002, Annual review of plant biology.

[67]  W. Briggs,et al.  Photoreceptors in plant photomorphogenesis to date. Five phytochromes, two cryptochromes, one phototropin, and one superchrome. , 2001, Plant physiology.

[68]  F. Smith,et al.  COLORIMETRIC METHOD FOR DETER-MINATION OF SUGAR AND RELATED SUBSTANCE , 1956 .