Flower Development under Drought Stress: Morphological and Transcriptomic Analyses Reveal Acute Responses and Long-Term Acclimation in Arabidopsis[C][W]

Drought dramatically affects plant reproductive development and crop yield, but previous research has primarily focused on vegetative development. This work uses a scheme that allows plant growth with limited water to study plant responses to drought during reproductive development. The authors examine floral developmental defects and identify key genes affecting this process. Drought dramatically affects plant growth and crop yield, but previous studies primarily examined responses to drought during vegetative development. Here, to study responses to drought during reproductive development, we grew Arabidopsis thaliana plants with limited water, under conditions that allowed the plants to initiate and complete reproduction. Drought treatment from just after the onset of flowering to seed maturation caused an early arrest of floral development and sterility. After acclimation, plants showed reduced fertility that persisted throughout reproductive development. Floral defects included abnormal anther development, lower pollen viability, reduced filament elongation, ovule abortion, and failure of flowers to open. Drought also caused differential expression of 4153 genes, including flowering time genes FLOWERING LOCUS T, SUPPRESSOR OF OVEREXPRESSION OF CO1, and LEAFY, genes regulating anther and pistil development, and stress-related transcription factors. Mutant phenotypes of hypersensitivity to drought and fewer differentially expressed genes suggest that DEHYDRATION RESPONSE ELEMENT B1A may have an important function in drought response in flowers. A more severe filament elongation defect under drought in myb21 plants demonstrated that appropriate stamen development requires MYB DOMAIN PROTEIN 21 under drought conditions. Our study reveals a regulatory cascade in reproductive responses and acclimation under drought.

[1]  C. Tonelli,et al.  GIGANTEA Enables Drought Escape Response via Abscisic Acid-Dependent Activation of the Florigens and SUPPRESSOR OF OVEREXPRESSION OF CONSTANS11[C][W] , 2013, Plant Physiology.

[2]  Arjun Krishnan,et al.  Effects of Drought on Gene Expression in Maize Reproductive and Leaf Meristem Tissue Revealed by RNA-Seq1[W][OA] , 2012, Plant Physiology.

[3]  P. Verslues,et al.  Unique Drought Resistance Functions of the Highly ABA-Induced Clade A Protein Phosphatase 2Cs1[W][OA] , 2012, Plant Physiology.

[4]  D. L. Wathugala,et al.  ERF5 and ERF6 Play Redundant Roles as Positive Regulators of JA/Et-Mediated Defense against Botrytis cinerea in Arabidopsis , 2012, PloS one.

[5]  C. D. de Oliveira,et al.  A combinatorial TIR1/AFB-Aux/IAA co-receptor system for differential sensing of auxin , 2012, Nature chemical biology.

[6]  C. Lata,et al.  Role of DREBs in regulation of abiotic stress responses in plants. , 2011, Journal of experimental botany.

[7]  Murray Grant,et al.  Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. , 2011, Annual review of phytopathology.

[8]  T. Juenger,et al.  Drought, metabolites, and Arabidopsis natural variation: a promising combination for understanding adaptation to water-limited environments. , 2011, Current opinion in plant biology.

[9]  R. Albert,et al.  Common and unique elements of the ABA-regulated transcriptome of Arabidopsis guard cells , 2011, BMC Genomics.

[10]  M. Van Montagu,et al.  Jasmonate signaling involves the abscisic acid receptor PYL4 to regulate metabolic reprogramming in Arabidopsis and tobacco , 2011, Proceedings of the National Academy of Sciences.

[11]  W. Peng,et al.  The Jasmonate-ZIM Domain Proteins Interact with the R2R3-MYB Transcription Factors MYB21 and MYB24 to Affect Jasmonate-Regulated Stamen Development in Arabidopsis[C][W] , 2011, Plant Cell.

[12]  J. Ward,et al.  Functional Properties of the Arabidopsis Peptide Transporters AtPTR1 and AtPTR5* , 2010, The Journal of Biological Chemistry.

[13]  Jian-Kang Zhu,et al.  ABA receptors: the START of a new paradigm in phytohormone signalling. , 2010, Journal of experimental botany.

[14]  Hideyuki Shimizu,et al.  Plant responses to drought and rewatering , 2010, Plant signaling & behavior.

[15]  R. Richards,et al.  Importance of pre-anthesis anther sink strength for maintenance of grain number during reproductive stage water stress in wheat. , 2010, Plant, cell & environment.

[16]  S. Cutler,et al.  Abscisic acid: emergence of a core signaling network. , 2010, Annual review of plant biology.

[17]  Zhou Du,et al.  agriGO: a GO analysis toolkit for the agricultural community , 2010, Nucleic Acids Res..

[18]  K. Shinozaki,et al.  'Omics' analyses of regulatory networks in plant abiotic stress responses. , 2010, Current opinion in plant biology.

[19]  N. C. Avanci,et al.  Jasmonates are phytohormones with multiple functions, including plant defense and reproduction. , 2010, Genetics and molecular research : GMR.

[20]  S. Assmann,et al.  Heterotrimeric G proteins regulate reproductive trait plasticity in response to water availability. , 2010, The New phytologist.

[21]  K. Shinozaki,et al.  AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation. , 2010, The Plant journal : for cell and molecular biology.

[22]  K. Shinozaki,et al.  Comprehensive analysis of rice DREB2-type genes that encode transcription factors involved in the expression of abiotic stress-responsive genes , 2010, Molecular Genetics and Genomics.

[23]  S. Cutler,et al.  A Gate-Latch-Lock Mechanism for Hormone Signaling by Abscisic Acid Receptors , 2009, Nature.

[24]  F. Myouga,et al.  Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis , 2009, Proceedings of the National Academy of Sciences.

[25]  Christian Jung,et al.  Flowering time control and applications in plant breeding. , 2009, Trends in plant science.

[26]  P. McCourt,et al.  Abscisic Acid Inhibits Type 2C Protein Phosphatases via the PYR/PYL Family of START Proteins , 2009, Science.

[27]  G. Jürgens,et al.  Survival of the flexible: hormonal growth control and adaptation in plant development , 2009, Nature Reviews Genetics.

[28]  Chuanyou Li,et al.  The RHA2a-interacting proteins ANAC019 and ANAC055 may play a dual role in regulating ABA response and jasmonate response , 2009 .

[29]  Zhiwei Cheng,et al.  Gibberellin Acts through Jasmonate to Control the Expression of MYB21, MYB24, and MYB57 to Promote Stamen Filament Growth in Arabidopsis , 2009, PLoS genetics.

[30]  Jonathan D. G. Jones,et al.  Role of plant hormones in plant defence responses , 2009, Plant Molecular Biology.

[31]  D. Fernandez,et al.  MIKC* MADS Domain Heterodimers Are Required for Pollen Maturation and Tube Growth in Arabidopsis1[W][OA] , 2009, Plant Physiology.

[32]  J. Flexas,et al.  Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. , 2009, Annals of botany.

[33]  S. Sengupta,et al.  Insight into the salt tolerance factors of a wild halophytic rice, Porteresia coarctata: a physiological and proteomic approach , 2009, Planta.

[34]  Frederick M. Ausubel,et al.  Glucosinolate Metabolites Required for an Arabidopsis Innate Immune Response , 2009, Science.

[35]  A. Mandaokar,et al.  MYB108 Acts Together with MYB24 to Regulate Jasmonate-Mediated Stamen Maturation in Arabidopsis1[OA] , 2008, Plant Physiology.

[36]  Sarah M Assmann,et al.  Functional Proteomics of Arabidopsis thaliana Guard Cells Uncovers New Stomatal Signaling Pathways[W][OA] , 2008, The Plant Cell Online.

[37]  J. Ehlting,et al.  Genome-wide and expression analysis of protein phosphatase 2C in rice and Arabidopsis , 2008, BMC Genomics.

[38]  Yi Wang,et al.  Transcriptome Analyses Show Changes in Gene Expression to Accompany Pollen Germination and Tube Growth in Arabidopsis1[W][OA] , 2008, Plant Physiology.

[39]  Y. Marco,et al.  RD19, an Arabidopsis Cysteine Protease Required for RRS1-R–Mediated Resistance, Is Relocalized to the Nucleus by the Ralstonia solanacearum PopP2 Effector[W] , 2008, The Plant Cell Online.

[40]  Hong Ma,et al.  Regulation of Arabidopsis early anther development by the mitogen-activated protein kinases, MPK3 and MPK6, and the ERECTA and related receptor-like kinases. , 2008, Molecular plant.

[41]  Q. Xie,et al.  Role of the Arabidopsis thaliana NAC transcription factors ANAC019 and ANAC055 in regulating jasmonic acid-signaled defense responses , 2008, Cell Research.

[42]  Yiyue Zhang,et al.  Targeted Degradation of the Cyclin-Dependent Kinase Inhibitor ICK4/KRP6 by RING-Type E3 Ligases Is Essential for Mitotic Cell Cycle Progression during Arabidopsis Gametogenesis[W][OA] , 2008, The Plant Cell Online.

[43]  Anthony L. Schilmiller,et al.  COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine , 2008, Proceedings of the National Academy of Sciences.

[44]  I. Hwang,et al.  Isolation and characterization of multiple abundant lipid transfer protein isoforms in developing sesame (Sesamum indicum L.) seeds. , 2008, Plant physiology and biochemistry : PPB.

[45]  V. Sundaresan,et al.  Cell-Fate Switch of Synergid to Egg Cell in Arabidopsis eostre Mutant Embryo Sacs Arises from Misexpression of the BEL1-Like Homeodomain Gene BLH1[W] , 2007, The Plant Cell Online.

[46]  K. Shinozaki,et al.  Perception and transduction of abscisic acid signals: keys to the function of the versatile plant hormone ABA. , 2007, Trends in plant science.

[47]  Hong Ma,et al.  Differential gene expression in Arabidopsis wild-type and mutant anthers: insights into anther cell differentiation and regulatory networks. , 2007, The Plant journal : for cell and molecular biology.

[48]  Brian C. Thomas,et al.  G-Boxes, Bigfoot Genes, and Environmental Response: Characterization of Intragenomic Conserved Noncoding Sequences in Arabidopsis[W] , 2007, The Plant Cell Online.

[49]  Marta Godoy,et al.  ABA Is an Essential Signal for Plant Resistance to Pathogens Affecting JA Biosynthesis and the Activation of Defenses in Arabidopsis[W] , 2007, The Plant Cell Online.

[50]  M. Endo,et al.  Premature progression of anther early developmental programs accompanied by comprehensive alterations in transcription during high-temperature injury in barley plants , 2007, Molecular Genetics and Genomics.

[51]  K. Shinozaki,et al.  Gene networks involved in drought stress response and tolerance. , 2006, Journal of experimental botany.

[52]  Hong Ma,et al.  Regulation of Arabidopsis tapetum development and function by DYSFUNCTIONAL TAPETUM1 (DYT1) encoding a putative bHLH transcription factor , 2006, Development.

[53]  K. Shinozaki,et al.  Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. , 2006, Current opinion in plant biology.

[54]  Joshua G. Steffen,et al.  AGL80 Is Required for Central Cell and Endosperm Development in Arabidopsis[W] , 2006, The Plant Cell Online.

[55]  Hong Ma,et al.  The BAM1/BAM2 Receptor-Like Kinases Are Important Regulators of Arabidopsis Early Anther Development[W] , 2006, The Plant Cell Online.

[56]  B. M. Lange,et al.  Transcriptional regulators of stamen development in Arabidopsis identified by transcriptional profiling. , 2006, The Plant journal : for cell and molecular biology.

[57]  Zichao Li,et al.  Genetic variation in the sensitivity of anther dehiscence to drought stress in rice , 2006 .

[58]  Kazuo Shinozaki,et al.  Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. , 2006, Annual review of plant biology.

[59]  Saranyan K. Palaniswamy,et al.  AGRIS and AtRegNet. A Platform to Link cis-Regulatory Elements and Transcription Factors into Regulatory Networks1[W][OA] , 2006, Plant Physiology.

[60]  T. D. Mitchell,et al.  Ecosystem Service Supply and Vulnerability to Global Change in Europe , 2005, Science.

[61]  S. Husted,et al.  Pollen development and fertilization in Arabidopsis is dependent on the MALE GAMETOGENESIS IMPAIRED ANTHERS gene encoding a type V P-type ATPase. , 2005, Genes & development.

[62]  Zhenbiao Yang,et al.  Oscillatory ROP GTPase activation leads the oscillatory polarized growth of pollen tubes. , 2005, Molecular biology of the cell.

[63]  K. Price,et al.  Regional vegetation die-off in response to global-change-type drought. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[64]  J. Boyer,et al.  Imaging and quantifying carbohydrate transport to the developing ovaries of maize. , 2005, Annals of botany.

[65]  Kelian Sun,et al.  Environmental stress alters genes expression and induces ovule abortion: reactive oxygen species appear as ovules commit to abort , 2005, Planta.

[66]  P. Yancey,et al.  Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses , 2005, Journal of Experimental Biology.

[67]  Lixi Jiang,et al.  Overexpression of TAPETUM DETERMINANT1 Alters the Cell Fates in the Arabidopsis Carpel and Tapetum via Genetic Interaction with EXCESS MICROSPOROCYTES1/EXTRA SPOROGENOUS CELLS1 , 2005, Plant Physiology.

[68]  Peter K Hepler,et al.  Pectin Methylesterase, a Regulator of Pollen Tube Growth1[w] , 2005, Plant Physiology.

[69]  Hong Ma.  Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. , 2005, Annual review of plant biology.

[70]  Erich Kombrink,et al.  A New Type of Peroxisomal Acyl-Coenzyme A Synthetase from Arabidopsis thaliana Has the Catalytic Capacity to Activate Biosynthetic Precursors of Jasmonic Acid* , 2005, Journal of Biological Chemistry.

[71]  K. Fischer,et al.  The Arabidopsis Plastidic Glucose 6-Phosphate/Phosphate Translocator GPT1 Is Essential for Pollen Maturation and Embryo Sac Development , 2005, The Plant Cell Online.

[72]  V. Sundaresan,et al.  VANGUARD1 Encodes a Pectin Methylesterase That Enhances Pollen Tube Growth in the Arabidopsis Style and Transmitting Tract , 2005, The Plant Cell Online.

[73]  Ana I. Caño-Delgado,et al.  Heterodimerization and Endocytosis of Arabidopsis Brassinosteroid Receptors BRI1 and AtSERK3 (BAK1) , 2004, The Plant Cell Online.

[74]  Wolfgang Busch,et al.  Identification of novel heat shock factor-dependent genes and biochemical pathways in Arabidopsis thaliana. , 2004, The Plant journal : for cell and molecular biology.

[75]  J. Boyer,et al.  Sugar-responsive gene expression, invertase activity, and senescence in aborting maize ovaries at low water potentials. , 2004, Annals of botany.

[76]  M. Westgate,et al.  Grain yields with limited water. , 2004, Journal of experimental botany.

[77]  Y. Zuily-Fodil,et al.  Effect of drought stress on lipid metabolism in the leaves of Arabidopsis thaliana (ecotype Columbia). , 2004, Annals of botany.

[78]  S. McCormick,et al.  A compendium of methods useful for characterizing Arabidopsis pollen mutants and gametophytically-expressed genes. , 2004, The Plant journal : for cell and molecular biology.

[79]  Kelian Sun,et al.  Ovule Abortion in Arabidopsis Triggered by Stress1 , 2004, Plant Physiology.

[80]  E. Meyerowitz,et al.  The homeotic protein AGAMOUS controls microsporogenesis by regulation of SPOROCYTELESS , 2004, Nature.

[81]  Kazuo Shinozaki,et al.  Identification of cold-inducible downstream genes of the Arabidopsis DREB1A/CBF3 transcriptional factor using two microarray systems. , 2004, The Plant journal : for cell and molecular biology.

[82]  R. Macknight,et al.  It's time to flower: the genetic control of flowering time , 2004, BioEssays : news and reviews in molecular, cellular and developmental biology.

[83]  K. Shinozaki,et al.  A combination of the Arabidopsis DREB1A gene and stress-inducible rd29A promoter improved drought- and low-temperature stress tolerance in tobacco by gene transfer. , 2004, Plant & cell physiology.

[84]  K. Oda,et al.  dwarf and delayed-flowering 1, a novel Arabidopsis mutant deficient in gibberellin biosynthesis because of overexpression of a putative AP2 transcription factor. , 2004, The Plant journal : for cell and molecular biology.

[85]  B. Hauser,et al.  The phenotype of Arabidopsis ovule mutants mimics the morphology of primitive seed plants , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[86]  Lixi Jiang,et al.  TAPETUM DETERMINANT1 Is Required for Cell Specialization in the Arabidopsis Anther Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.016618. , 2003, The Plant Cell Online.

[87]  S. Luan.  Protein phosphatases in plants. , 2003, Annual review of plant biology.

[88]  K. Shinozaki,et al.  Regulatory network of gene expression in the drought and cold stress responses. , 2003, Current opinion in plant biology.

[89]  G. Ditta,et al.  Assessing the redundancy of MADS-box genes during carpel and ovule development , 2003, Nature.

[90]  D. Horner,et al.  Molecular and Phylogenetic Analyses of the Complete MADS-Box Transcription Factor Family in Arabidopsis Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.011544. , 2003, The Plant Cell Online.

[91]  M. Andersen,et al.  Loss of pod set caused by drought stress is associated with water status and ABA content of reproductive structures in soybean. , 2003, Functional plant biology : FPB.

[92]  Hur-Song Chang,et al.  Transcriptome Changes for Arabidopsis in Response to Salt, Osmotic, and Cold Stress1,212 , 2002, Plant Physiology.

[93]  H. Dickinson,et al.  EXS, a Putative LRR Receptor Kinase, Regulates Male Germline Cell Number and Tapetal Identity and Promotes Seed Development in Arabidopsis , 2002, Current Biology.

[94]  K. Koch,et al.  Soluble Invertase Expression Is an Early Target of Drought Stress during the Critical, Abortion-Sensitive Phase of Young Ovary Development in Maize1 , 2002, Plant Physiology.

[95]  M. Thomashow,et al.  Transcription Factor CBF4 Is a Regulator of Drought Adaptation in Arabidopsis1 , 2002, Plant Physiology.

[96]  Hong Ma,et al.  The excess microsporocytes1 gene encodes a putative leucine-rich repeat receptor protein kinase that controls somatic and reproductive cell fates in the Arabidopsis anther. , 2002, Genes & development.

[97]  Jian-Kang Zhu,et al.  Cell Signaling during Cold, Drought, and Salt Stress Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.000596. , 2002, The Plant Cell Online.

[98]  Karam B. Singh,et al.  Identification of Arabidopsis Ethylene-Responsive Element Binding Factors with Distinct Induction Kinetics after Pathogen Infection1,212 , 2002, Plant Physiology.

[99]  D. Bouchez,et al.  Pollen tube development and competitive ability are impaired by disruption of a Shaker K(+) channel in Arabidopsis. , 2002, Genes & development.

[100]  C. Staiger.  Faculty Opinions recommendation of A genome-wide analysis of Arabidopsis Rop-interactive CRIB motif-containing proteins that act as Rop GTPase targets. , 2002 .

[101]  P. Tighe,et al.  The Arabidopsis MALE STERILITY1 (MS1) gene is a transcriptional regulator of male gametogenesis, with homology to the PHD-finger family of transcription factors. , 2001, The Plant journal : for cell and molecular biology.

[102]  J. Görlach,et al.  Growth Stage–Based Phenotypic Analysis of Arabidopsis , 2001, The Plant Cell Online.

[103]  T. Setter,et al.  Water deficit inhibits cell division and expression of transcripts involved in cell proliferation and endoreduplication in maize endosperm. , 2001, Journal of experimental botany.

[104]  D. Weigel,et al.  A Molecular Link between Stem Cell Regulation and Floral Patterning in Arabidopsis , 2001, Cell.

[105]  Y. Choi,et al.  Jasmonic acid carboxyl methyltransferase: A key enzyme for jasmonate-regulated plant responses , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[106]  Hong Wang,et al.  Gene Expression Profiles during the Initial Phase of Salt Stress in Rice , 2001, Plant Cell.

[107]  Koji Goto,et al.  Complexes of MADS-box proteins are sufficient to convert leaves into floral organs , 2001, Nature.

[108]  K. Shinozaki,et al.  Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[109]  G. Ditta,et al.  B and C floral organ identity functions require SEPALLATA MADS-box genes , 2000, Nature.

[110]  Yuval Eshed,et al.  SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis , 2000, Nature.

[111]  M. Ohme-Takagi,et al.  Arabidopsis Ethylene-Responsive Element Binding Factors Act as Transcriptional Activators or Repressors of GCC Box–Mediated Gene Expression , 2000, Plant Cell.

[112]  P. Sieber,et al.  Molecular analysis of NOZZLE, a gene involved in pattern formation and early sporogenesis during sex organ development in Arabidopsis thaliana. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[113]  V. Sundaresan,et al.  The SPOROCYTELESS gene of Arabidopsis is required for initiation of sporogenesis and encodes a novel nuclear protein. , 1999, Genes & development.

[114]  L. R. Dillenburg,et al.  MEASUREMENTS OF LEAF RELATIVE WATER CONTENT IN ARAUCARIA ANGUSTIFOLIA 1 , 1999 .

[115]  Heiko Schoof,et al.  Role of WUSCHEL in Regulating Stem Cell Fate in the Arabidopsis Shoot Meristem , 1998, Cell.

[116]  K. Yamaguchi-Shinozaki,et al.  An Arabidopsis gene family encoding DRE/CRT binding proteins involved in low-temperature-responsive gene expression. , 1998, Biochemical and biophysical research communications.

[117]  K. Shinozaki,et al.  Two Transcription Factors, DREB1 and DREB2, with an EREBP/AP2 DNA Binding Domain Separate Two Cellular Signal Transduction Pathways in Drought- and Low-Temperature-Responsive Gene Expression, Respectively, in Arabidopsis , 1998, Plant Cell.

[118]  June I. Medford,et al.  A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis , 1996, Nature.

[119]  W. Peacock,et al.  Differential Interactions of Promoter Elements in Stress Responses of the Arabidopsis Adh Gene , 1994, Plant physiology.

[120]  R. E. Sharp,et al.  Growth of the Maize Primary Root at Low Water Potentials : III. Role of Increased Proline Deposition in Osmotic Adjustment. , 1991, Plant physiology.

[121]  R. E. Sharp,et al.  Growth of the Maize Primary Root at Low Water Potentials : II. Role of Growth and Deposition of Hexose and Potassium in Osmotic Adjustment. , 1990, Plant physiology.

[122]  J. Bowman,et al.  Early flower development in Arabidopsis. , 1990, The Plant cell.

[123]  R. Gleadow,et al.  Effect of Post-anthesis Drought on Cell Division and Starch Accumulation in Developing Wheat Grains , 1985 .

[124]  D. Lloyd.  SEXUAL STRATEGIES IN PLANTS , 1980 .

[125]  G. Bingham,et al.  Rapid estimates of relative water content. , 1974, Plant physiology.

[126]  Tracey Ann Cuin,et al.  Plant Salt Tolerance , 2012, Methods in Molecular Biology.

[127]  M. Farooq,et al.  Plant drought stress: effects, mechanisms and management , 2011, Agronomy for Sustainable Development.

[128]  SnRK,et al.  In vitro reconstitution of an abscisic acid signalling pathway , 2009 .

[129]  Joop J A van Loon,et al.  Role of glucosinolates in insect-plant relationships and multitrophic interactions. , 2009, Annual review of entomology.

[130]  Thomas Rausch,et al.  Elaborate spatial patterning of cell-wall PME and PMEI at the pollen tube tip involves PMEI endocytosis, and reflects the distribution of esterified and de-esterified pectins. , 2008, The Plant journal : for cell and molecular biology.

[131]  K. Shinozaki,et al.  Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. , 2006, Plant & cell physiology.

[132]  C. Périlleux,et al.  A physiological overview of the genetics of flowering time control. , 2005, Plant biotechnology journal.

[133]  H. Saini,et al.  Drought-induced male sterility in rice: Changes in carbohydrate levels and enzyme activities associated with the inhibition of starch accumulation in pollen , 2005, Sexual Plant Reproduction.

[134]  Guohai Wu,et al.  A lipid transfer protein gene BG-14 is differentially regulated by abiotic stress, ABA, anisomycin, and sphingosine in bromegrass (Bromus inermis). , 2004, Journal of plant physiology.

[135]  P. Huijser,et al.  The Arabidopsis ABORTED MICROSPORES (AMS) gene encodes a MYC class transcription factor. , 2003, The Plant journal : for cell and molecular biology.

[136]  Shoshi Kikuchi,et al.  Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana. , 2003, DNA research : an international journal for rapid publication of reports on genes and genomes.

[137]  Jian-Kang Zhu,et al.  Salt and drought stress signal transduction in plants. , 2002, Annual review of plant biology.

[138]  H. Saini.  Effects of water stress on male gametophyte development in plants , 1997, Sexual Plant Reproduction.

[139]  Sylvie Lalonde,et al.  Early signs of disruption of wheat anther development associated with the induction of male sterility by meiotic-stage water deficit , 1997, Sexual Plant Reproduction.

[140]  Charles Elkan,et al.  Fitting a Mixture Model By Expectation Maximization To Discover Motifs In Biopolymer , 1994, ISMB.

[141]  D. Lloyd.  I. AN HYPOTHESIS OF SERIAL ADJUSTMENT OF MATERNAL INVESTMENT DURING ONE REPRODUCTIVE SESSION , 1980 .

[142]  M. P. Alexander.  Differential staining of aborted and nonaborted pollen. , 1969, Stain technology.