Seed dormancy release in Arabidopsis Cvi by dry after-ripening, low temperature, nitrate and light shows common quantitative patterns of gene expression directed by environmentally specific sensing.

The depth of seed dormancy can be influenced by a number of different environmental signals, but whether a common mechanism underlies this apparently similar response has yet to be investigated. Full-genome microarrays were used for a global transcript analysis of Arabidopsis thaliana Cape Verde Island accession seeds exposed to dry after-ripening (AR), or low temperature, nitrate and light when imbibed. Germination studies showed that the sensitivity of imbibed seeds to low temperature, nitrate and light was dependent upon the length of time spent AR following harvest. Seeds had an absolute requirement for light to complete dormancy release in all conditions, but this effect required an exposure to a prior dormancy relieving environment. Principal component analyses of the expression patterns observed grouped physiological states in a way that related to the depth of seed dormancy, rather than the type of environmental exposure. Furthermore, opposite changes in transcript abundance of genes in sets associated with dormancy, or dormancy relief through AR, were also related to the depth of dormancy and common to different environments. Besides these common quantitative changes, environment-specific gene expression patterns during dormancy relief are also described. For example, higher transcript abundance for genes linked to the process of nitrate accumulation, and nitrate reduction was associated with dormancy relief. The quantity of GA3ox1 transcripts increased during dormancy relief in all conditions, in particular when dormancy relief was completed by exposure to light. This contrasts with transcripts linked to abscisic acid (ABA) synthesis, which declined. The results are consistent with a role for the ABA/gibberellic acid balance in integrating dormancy-relieving environmental signals.

[1]  M. Koornneef,et al.  Cloning of DOG1, a quantitative trait locus controlling seed dormancy in Arabidopsis , 2006, Proceedings of the National Academy of Sciences.

[2]  K. Thompson,et al.  Seeds: Physiology of Development and Germination , 1986 .

[3]  T. Wilkins,et al.  A modified hot borate method significantly enhances the yield of high-quality RNA from cotton (Gossypium hirsutum L.). , 1994, Analytical biochemistry.

[4]  M. Wagner,et al.  Changes in endogenous abscisic acid levels during dormancy release and maintenance of mature seeds: studies with the Cape Verde Islands ecotype, the dormant model of Arabidopsis thaliana , 2004, Planta.

[5]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[6]  Philippe Lucas,et al.  Gene expression analysis by cDNA-AFLP highlights a set of new signaling networks and translational control during seed dormancy breaking in Nicotiana plumbaginifolia , 2005, Plant Molecular Biology.

[7]  Ayuko Kuwahara,et al.  Gibberellin Biosynthesis and Response during Arabidopsis Seed Germination Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.011650. , 2003, The Plant Cell Online.

[8]  C. Baskin,et al.  Seeds: Ecology, Biogeography, and, Evolution of Dormancy and Germination , 1998 .

[9]  C. M. Karssen,et al.  Gibberellins in seeds of Arabidopsis thaliana: biological activities, identification and effects of light and chilling on endogenous levels , 1994, Plant Growth Regulation.

[10]  Jean YH Yang,et al.  Bioconductor: open software development for computational biology and bioinformatics , 2004, Genome Biology.

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

[12]  A. Leopold,et al.  Relationship between water content and afterripening in-red rice , 1988 .

[13]  M. Koornneef,et al.  Gibberellin requirement for Arabidopsis seed germination is determined both by testa characteristics and embryonic abscisic acid. , 2000, Plant physiology.

[14]  C. M. Karssen,et al.  Nitrate Reductase Independent Stimulation of Seed Germination in Sisymbrium officinale L. (Hedge Mustard) by Light and Nitrate , 1989 .

[15]  S Rozen,et al.  Primer3 on the WWW for general users and for biologist programmers. , 2000, Methods in molecular biology.

[16]  H. Kawaide,et al.  Phytochrome regulates gibberellin biosynthesis during germination of photoblastic lettuce seeds. , 1998, Plant physiology.

[17]  M. Delledonne NO news is good news for plants. , 2005, Current opinion in plant biology.

[18]  W. Finch-Savage,et al.  Seed dormancy and the control of germination. , 2006, The New phytologist.

[19]  K. Halliday,et al.  Cold and Light Control Seed Germination through the bHLH Transcription Factor SPATULA , 2005, Current Biology.

[20]  M. Fenner,et al.  The role of temperature in the regulation of seed dormancy and germination. , 2000 .

[21]  Yuji Kamiya,et al.  Genome-wide profiling of stored mRNA in Arabidopsis thaliana seed germination: epigenetic and genetic regulation of transcription in seed. , 2005, The Plant journal : for cell and molecular biology.

[22]  K. Thompson,et al.  The Ecology of Seeds: References , 2005 .

[23]  Ken Thompson,et al.  The Ecology of Seeds by Michael Fenner , 2005 .

[24]  Jungwon Yoon,et al.  The Arabidopsis Information Resource (TAIR): a model organism database providing a centralized, curated gateway to Arabidopsis biology, research materials and community , 2003, Nucleic Acids Res..

[25]  B. Winkel-Shirley,et al.  Interactions among enzymes of the Arabidopsis flavonoid biosynthetic pathway. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[26]  A. Murphy,et al.  Flavonoids act as negative regulators of auxin transport in vivo in arabidopsis. , 2001, Plant physiology.

[27]  S. Meyer,et al.  A hydrothermal after-ripening time model for seed dormancy loss in Bromus tectorum L. , 2006, Seed Science Research.

[28]  K. Donohue,et al.  Seeds and seasons: interpreting germination timing in the field , 2005, Seed Science Research.

[29]  F. Gubler,et al.  Dormancy of Arabidopsis seeds and barley grains can be broken by nitric oxide , 2004, Planta.

[30]  N. Kruger,et al.  The oxidative pentose phosphate pathway: structure and organisation. , 2003, Current opinion in plant biology.

[31]  S. Goldman,et al.  Microarray analysis of nitric oxide responsive transcripts in Arabidopsis. , 2004, Plant biotechnology journal.

[32]  J. Vandekerckhove,et al.  The Effect of α-Amanitin on the Arabidopsis Seed Proteome Highlights the Distinct Roles of Stored and Neosynthesized mRNAs during Germination1 , 2004, Plant Physiology.

[33]  K. Thompson,et al.  The functional ecology of soil seed banks. , 2000 .

[34]  I. Baldwin,et al.  Smoke exposure alters endogenous gibberellin and abscisic acid pools and gibberellin sensitivity while eliciting germination in the post-fire annual, Nicotiana attenuata , 2004, Seed Science Research.

[35]  Rongchen Wang,et al.  Genomic Analysis of a Nutrient Response in Arabidopsis Reveals Diverse Expression Patterns and Novel Metabolic and Potential Regulatory Genes Induced by Nitrate , 2000, Plant Cell.

[36]  P. Toorop,et al.  Gene expression profiles of Arabidopsis Cvi seeds during dormancy cycling indicate a common underlying dormancy control mechanism. , 2006, The Plant journal : for cell and molecular biology.

[37]  J. Ecker,et al.  Type-A Arabidopsis Response Regulators Are Partially Redundant Negative Regulators of Cytokinin Signaling Online version contains Web-only data. , 2004, The Plant Cell Online.

[38]  Xing Wang Deng,et al.  Molecular interaction between COP1 and HY5 defines a regulatory switch for light control of Arabidopsis development. , 1998, Molecular cell.

[39]  John B. Anderson,et al.  CDD: a Conserved Domain Database for protein classification , 2004, Nucleic Acids Res..

[40]  C. M. Karssen,et al.  Redefining seed dormancy: an attempt to integrate physiology and ecology , 1995 .

[41]  G. Sessa,et al.  The Arabidopsis Athb-2 and -4 genes are strongly induced by far-red-rich light. , 1993, The Plant journal : for cell and molecular biology.

[42]  N. Crawford Mechanisms for nitric oxide synthesis in plants. , 2006, Journal of experimental botany.

[43]  Ulf-Ingo Flügge,et al.  The Plastidic Pentose Phosphate Translocator Represents a Link between the Cytosolic and the Plastidic Pentose Phosphate Pathways in Plants1 , 2002, Plant Physiology.

[44]  A. Poustka,et al.  Parameter estimation for the calibration and variance stabilization of microarray data , 2003, Statistical applications in genetics and molecular biology.

[45]  H. Hilhorst Dose-Response Analysis of Factors Involved in Germination and Secondary Dormancy of Seeds of Sisymbrium officinale: I. Phytochrome. , 1990, Plant physiology.

[46]  A. Mead,et al.  One-step analysis of seed storage data and the longevity of Arabidopsis thaliana seeds. , 2003, Journal of experimental botany.

[47]  Roland Arnold,et al.  MIPS Arabidopsis thaliana Database (MAtDB): an integrated biological knowledge resource based on the first complete plant genome , 2002, Nucleic Acids Res..

[48]  J. Casal,et al.  Phytochromes and seed germination , 1998, Seed Science Research.

[49]  A. Peeters,et al.  The genetics of seed dormancy in Arabidopsis thaliana. , 2000 .

[50]  Ken Thompson,et al.  The Ecology of Seeds: Contents , 2005 .

[51]  R. Gallagher,et al.  Dormancy release in Lolium rigidum seeds is a function of thermal after-ripening time and seed water content. , 2003, Functional plant biology : FPB.

[52]  Gerhard Leubner-Metzger,et al.  Plant hormone interactions during seed dormancy release and germination , 2005, Seed Science Research.

[53]  M. Cohn Operational and philosophical decisions in seed dormancy research , 1996, Seed Science Research.

[54]  Yuji Kamiya,et al.  Activation of Gibberellin Biosynthesis and Response Pathways by Low Temperature during Imbibition of Arabidopsis thaliana Seeds On-line version contains Web-only data. , 2004, The Plant Cell Online.

[55]  K. L. Poff,et al.  The effects of potassium nitrate and NO-donors on phytochrome A- and phytochrome B-specific induced germination of Arabidopsis thaliana seeds , 2002, Seed Science Research.

[56]  I. Bancroft,et al.  Natural variation for seed oil composition in Arabidopsis thaliana. , 2003, Phytochemistry.

[57]  C. M. Karssen,et al.  Seed dormancy and germination: the role of abscisic acid and gibberellins and the importance of hormone mutants , 1992, Plant Growth Regulation.

[58]  H. Truong,et al.  Nitrate, a signal relieving seed dormancy in Arabidopsis. , 2005, Plant, cell & environment.

[59]  Tai-Ping Sun,et al.  Gibberellin signaling: biosynthesis, catabolism, and response pathways. , 2002, The Plant cell.

[60]  C. Baskin,et al.  A classification system for seed dormancy , 2004, Seed Science Research.

[61]  J. Bewley,et al.  Seed Germination and Dormancy. , 1997, The Plant cell.

[62]  Nick James,et al.  NASCArrays: a repository for microarray data generated by NASC's transcriptomics service , 2004, Nucleic Acids Res..