The Cape Verde Islands Allele of Cryptochrome 2 Enhances Cotyledon Unfolding in the Absence of Blue Light in Arabidopsis1[w]

We analyzed the natural genetic variation between Landsburg erecta (Ler) and Cape Verde Islands (Cvi) accessions by studying 105 recombinant inbred lines to search for players in the regulation of sensitivity to light signals perceived by phytochromes in etiolated seedlings of Arabidopsis. In seedlings grown under hourly pulses of far-red (FR) light, we identified three quantitative trait loci (QTLs; VLF3, VLF4, and VLF5) for hypocotyl growth inhibition and three different QTLs (VLF6, VLF7, and VLF1) for cotyledon unfolding. This indicates that different physiological outputs have selective regulation of sensitivity during de-etiolation. Ler alleles, compared with Cvi alleles, of VLF3, VLF4, VLF5, VLF7, and VLF1 enhanced, whereas the Ler allele of VLF6 reduced, the response to pulses of FR. We confirmed and narrowed down the position of some QTLs by using near-isogenic lines. VLF6 mapped close to the CRY2 (cryptochrome 2) gene. Transgenic Ler seedlings expressing the Cvi allele of CRY2 showed enhanced cotyledon unfolding under hourly pulses of FR compared with the wild type or transgenics expressing the CRY2-Ler allele. This response required phytochrome A. The cry1 cry2 double mutant lacking both cryptochromes showed reduced cotyledon unfolding under FR pulses. Because the CRY2-Cvi is a gain-of-function allele compared with CRY2-Ler, cryptochrome activity correlates positively with cotyledon unfolding under FR pulses. We conclude that the blue light photoreceptor cryptochrome 2 can modulate seedling photomorphogenesis in the absence of blue light. In addition to the nuclear loci, we identified cytoplasmic effects on seedling de-etiolation.

[1]  B. Thomas,et al.  Evidence for two photoreceptors controlling growth in de-etiolated seedlings , 1979, Planta.

[2]  J. Casal,et al.  Light, phytochrome signalling and photomorphogenesis in Arabidopsis , 2003, Photochemical & photobiological sciences : Official journal of the European Photochemistry Association and the European Society for Photobiology.

[3]  M. Koornneef,et al.  Analysis of natural allelic variation at seed dormancy loci of Arabidopsis thaliana. , 2003, Genetics.

[4]  J. Maloof.  QTL for plant growth and morphology. , 2003, Current opinion in plant biology.

[5]  M. Yanovsky,et al.  Missense Mutation in the PAS2 Domain of Phytochrome A Impairs Subnuclear Localization and a Subset of Responses Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.000521. , 2002, The Plant Cell Online.

[6]  M. Yanovsky,et al.  The Serine-Rich N-Terminal Domain of Oat Phytochrome A Helps Regulate Light Responses and Subnuclear Localization of the Photoreceptor1 , 2002, Plant Physiology.

[7]  J. Casal,et al.  SPA1, a component of phytochrome A signal transduction, regulates the light signaling current , 2002, Planta.

[8]  Paul Galland,et al.  Action Spectrum for Cryptochrome-Dependent Hypocotyl Growth Inhibition in Arabidopsis1 , 2002, Plant Physiology.

[9]  J. Christie,et al.  Phototropins 1 and 2: versatile plant blue-light receptors. , 2002, Trends in plant science.

[10]  J. Chory,et al.  Signal Transduction between the Chloroplast and the Nucleus Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010446. , 2002, The Plant Cell Online.

[11]  O. Loudet,et al.  Bay-0 × Shahdara recombinant inbred line population: a powerful tool for the genetic dissection of complex traits in Arabidopsis , 2002, Theoretical and Applied Genetics.

[12]  Detlef Weigel,et al.  Quantitative trait loci controlling light and hormone response in two accessions of Arabidopsis thaliana. , 2002, Genetics.

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

[14]  M. Yanovsky,et al.  Brassinosteroid mutants uncover fine tuning of phytochrome signaling. , 2002, Plant physiology.

[15]  J. Botto,et al.  Differential genetic variation in adaptive strategies to a common environmental signal in Arabidopsis accessions: phytochrome‐mediated shade avoidance , 2002 .

[16]  A. Brice,et al.  A QTL for flowering time in Arabidopsis reveals a novel allele of CRY2 , 2002, Nature Genetics.

[17]  A. Peeters,et al.  A QTL for flowering time in Arabidopsis reveals a novel allele of CRY2 , 2001, Nature Genetics.

[18]  M. Yanovsky,et al.  Resetting of the Circadian Clock by Phytochromes and Cryptochromes in Arabidopsis , 2001, Journal of biological rhythms.

[19]  J. Chory,et al.  Natural variation in light sensitivity of Arabidopsis , 2001, Nature Genetics.

[20]  K. Folta,et al.  Opposing roles of phytochrome A and phytochrome B in early cryptochrome-mediated growth inhibition. , 2001, The Plant journal : for cell and molecular biology.

[21]  J. Casal,et al.  Hierarchical coupling of phytochromes and cryptochromes reconciles stability and light modulation of Arabidopsis development. , 2001, Development.

[22]  K. Folta,et al.  Unexpected roles for cryptochrome 2 and phototropin revealed by high-resolution analysis of blue light-mediated hypocotyl growth inhibition. , 2001, The Plant journal : for cell and molecular biology.

[23]  S. G. Møller,et al.  A plastidic ABC protein involved in intercompartmental communication of light signaling. , 2001, Genes & development.

[24]  S. Kay,et al.  Cryptochromes Are Required for Phytochrome Signaling to the Circadian Clock but Not for Rhythmicity , 2000, Plant Cell.

[25]  Yan Liu,et al.  The C Termini of Arabidopsis Cryptochromes Mediate a Constitutive Light Response , 2000, Cell.

[26]  M. Yanovsky,et al.  A quadruple photoreceptor mutant still keeps track of time , 2000, Current Biology.

[27]  J. Casal,et al.  Sustained but Not Transient Phytochrome A Signaling Targets a Region of an Lhcb1*2 Promoter Not Necessary for Phytochrome B Action , 2000, Plant Cell.

[28]  M. Yanovsky,et al.  fhy3-1 retains inductive responses of phytochrome A. , 2000, Plant physiology.

[29]  J. Casal,et al.  Phytochromes, Cryptochromes, Phototropin: Photoreceptor Interactions in Plants , 2000, Photochemistry and photobiology.

[30]  M Koornneef,et al.  Naturally occurring variation in Arabidopsis: an underexploited resource for plant genetics. , 2000, Trends in plant science.

[31]  E. Spalding,et al.  Sequential and coordinated action of phytochromes A and B during Arabidopsis stem growth revealed by kinetic analysis. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[32]  R. Amasino,et al.  Natural allelic variation identifies new genes in the Arabidopsis circadian system. , 1999, The Plant journal : for cell and molecular biology.

[33]  M. Yanovsky,et al.  Regulation of phytochrome B signaling by phytochrome A and FHY1 in Arabidopsis thaliana. , 1999, The Plant journal : for cell and molecular biology.

[34]  A. Cashmore,et al.  Cryptochromes: blue light receptors for plants and animals. , 1999, Science.

[35]  D. V. Leenen,et al.  Mammalian Cry1 and Cry2 are essential for maintenance of circadian rhythms , 1999, Nature.

[36]  M. Koornneef,et al.  Natural allelic variation at seed size loci in relation to other life history traits of Arabidopsis thaliana. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[37]  G. Coupland,et al.  Analysis of natural allelic variation at flowering time loci in the Landsberg erecta and Cape Verde Islands ecotypes of Arabidopsis thaliana. , 1998, Genetics.

[38]  M Koornneef,et al.  Development of an AFLP based linkage map of Ler, Col and Cvi Arabidopsis thaliana ecotypes and construction of a Ler/Cvi recombinant inbred line population. , 1998, The Plant journal : for cell and molecular biology.

[39]  T. Mockler,et al.  Enhancement of blue-light sensitivity of Arabidopsis seedlings by a blue light receptor cryptochrome 2. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[40]  J. Casal.  Review article. Modes of action of phytochromes , 1998 .

[41]  J. Botto,et al.  Modes of action of phytochromes , 1998 .

[42]  K. Chase,et al.  Epistat : a computer program for identifying and testing interactions between pairs of quantitative trait loci , 1997, Theoretical and Applied Genetics.

[43]  S. Mathews,et al.  Phytochrome gene diversity , 1997 .

[44]  Garry C. Whitelam,et al.  The shade avoidance syndrome: multiple responses mediated by multiple phytochromes , 1997 .

[45]  J. Casal,et al.  Dual effect of phytochrome A on hypocotyl growth under continuous red light , 1997 .

[46]  M. Yanovsky,et al.  The VLF loci, polymorphic between ecotypes Landsberg erecta and Columbia, dissect two branches of phytochrome A signal transduction that correspond to very-low-fluence and high-irradiance responses. , 1997, The Plant journal : for cell and molecular biology.

[47]  M. Ahmad,et al.  Association of flavin adenine dinucleotide with the Arabidopsis blue light receptor CRY1 , 1995, Science.

[48]  M. Yanovsky,et al.  Phytochrome A, phytochrome B and HY4 are involved in hypocotyl growth responses to natural radiation in Arabidopsis: weak de‐etiolation of the phyA mutant under dense canopies , 1995 .

[49]  J. Casal,et al.  Overexpression of oat phytochrome A gene differentially affects stem growth responses to red/far‐red ratio signals characteristic of sparse or dense canopies , 1994 .

[50]  J. Chory,et al.  Phytochrome A and Phytochrome B Have Overlapping but Distinct Functions in Arabidopsis Development , 1994, Plant physiology.

[51]  J. Ecker,et al.  Assignment of 30 microsatellite loci to the linkage map of Arabidopsis. , 1994, Genomics.

[52]  A. Cashmore,et al.  HY4 gene of A. thaliana encodes a protein with characteristics of a blue-light photoreceptor , 1993, Nature.

[53]  M. L. Anderson,et al.  Phytochrome A null mutants of Arabidopsis display a wild-type phenotype in white light. , 1993, The Plant cell.

[54]  M. Koornneef,et al.  Genetic control of light-inhibited hypocotyl elongation in Arabidopsis thaliana (L.) , 1980 .

[55]  C. Cockerham,et al.  Maternal and Reciprocal Effects on Seedling Characters in ARABIDOPSIS THALIANA (L.) Heynh. , 1976, Genetics.