Transcriptomic analysis of Chinese yam (Dioscorea polystachya Turcz.) variants indicates brassinosteroid involvement in tuber development

Dioscorea is an important but underutilized genus of flowering plants that grows predominantly in tropical and subtropical regions. Several species, known as yam, develop large underground tubers and aerial bulbils that are used as food. The Chinese yam (D. polystachya Turcz.) is one of the few Dioscorea species that grows well in temperate regions and has been proposed as a climate-resilient crop to enhance food security in Europe. However, the fragile, club-like tubers are unsuitable for mechanical harvesting, which is facilitated by shorter and thicker storage organs. Brassinosteroids (BRs) play a key role in plant cell division, cell elongation and proliferation, as well as in the gravitropic response. We collected RNA-Seq data from the head, middle and tip of two tuber shape variants: F60 (long, thin) and F2000 (short, thick). Comparative transcriptome analysis of F60 vs. F2000 revealed 30,229 differentially expressed genes (DEGs), 1,393 of which were differentially expressed in the growing tip. Several DEGs are involved in steroid/BR biosynthesis or signaling, or may be regulated by BRs. The quantification of endogenous BRs revealed higher levels of castasterone (CS), 28-norCS, 28-homoCS and brassinolide in F2000 compared to F60 tubers. The highest BR levels were detected in the growing tip, and CS was the most abundant (439.6 ± 196.41 pmol/g in F2000 and 365.6 ± 112.78 pmol/g in F60). Exogenous 24-epi-brassinolide (epi-BL) treatment (20 nM) in an aeroponic system significantly increased the width-to-length ratio (0.045 ± 0.002) compared to the mock-treated plants (0.03 ± 0.002) after 7 weeks, indicating that exogenous epi-BL produces shorter and thicker tubers. In this study we demonstrate the role of BRs in D. polystachya tuber shape, providing insight into the role of plant hormones in yam storage organ development. We found that BRs can influence tuber shape in Chinese yam by regulating the expression of genes involved cell expansion. Our data can help to improve the efficiency of Chinese yam cultivation, which could provide an alternative food source and thus contribute to future food security in Europe.

[1]  Min Shen,et al.  Transcriptomic and physiological analysis reveal phytohormone and phenylpropanoid biosynthesis in root of Cynanchum auriculatum , 2023, Plant Growth Regulation.

[2]  S. Okamoto,et al.  Comparative transcriptome analysis during tuberous stem formation in Kohlrabi (B. oleracea var. gongylodes) at early growth periods (seedling stages). , 2022, Physiologia plantarum.

[3]  Wei Luo,et al.  StOFP20 regulates tuber shape and interacts with TONNEAU1 Recruiting Motif proteins in potato , 2022, Journal of Integrative Agriculture.

[4]  Yingfang Zhu,et al.  BIN2 phosphorylates the Thr280 of CO to restrict its function in promoting Arabidopsis flowering , 2022, bioRxiv.

[5]  Y. Bi,et al.  Brassinosteroid Accelerates Wound Healing of Potato Tubers by Activation of Reactive Oxygen Metabolism and Phenylpropanoid Metabolism , 2022, Foods.

[6]  Xiaofeng Wang,et al.  RNA interference knockdown of the brassinosteroid receptor BRI1 in potato (Solanum tuberosum L.) reveals novel functions for brassinosteroid signaling in controlling tuberization , 2021 .

[7]  Jun Liu,et al.  Modulation of JA signalling reveals the influence of StJAZ1-like on tuber initiation and tuber bulking in potato. , 2021, The Plant journal : for cell and molecular biology.

[8]  Zhenbiao Yang,et al.  TMK-based cell-surface auxin signalling activates cell-wall acidification , 2021, Nature.

[9]  Wei Wang,et al.  Brassinosteroids promote parenchyma cell and secondary xylem development in sugar beet ( Beta vulgaris L.) root , 2021, Plant direct.

[10]  Liping Jin,et al.  Genes related to circadian rhythm are involved in regulating tuberization time in potato , 2021, Horticultural Plant Journal.

[11]  Luonan Chen,et al.  Dynamic network biomarker analysis discovers IbNAC083 in initiation and regulation of sweet potato root tuberization. , 2021, The Plant journal : for cell and molecular biology.

[12]  Yuting Li,et al.  Regulatory mechanism of GA3 on tuber growth by DELLA-dependent pathway in yam (Dioscorea opposita) , 2021, Plant Molecular Biology.

[13]  Filip Vandenbussche,et al.  Brassinosteroids Influence Arabidopsis Hypocotyl Graviresponses Through Changes In Mannans And Cellulose. , 2021, Plant & cell physiology.

[14]  O. Borsani,et al.  The Arabidopsis TETRATRICOPEPTIDE THIOREDOXIN-LIKE 1 Gene Is Involved in Anisotropic Root Growth during Osmotic Stress Adaptation , 2021, Genes.

[15]  J. Epping,et al.  An underutilized orphan tuber crop—Chinese yam : a review , 2020, Planta.

[16]  G. Pasquali,et al.  EgPHI-1, a PHOSPHATE-INDUCED-1 gene from Eucalyptus globulus, is involved in shoot growth, xylem fiber length and secondary cell wall properties , 2020, Planta.

[17]  Wei Wang,et al.  Brassinosteroids Promote Parenchyma Cell and Secondary Xylem Development in Sugar Beet (Beta vulgaris L.) Root , 2020, bioRxiv.

[18]  Damian Gruszka,et al.  Comprehensive Overview of the Brassinosteroid Biosynthesis Pathways: Substrates, Products, Inhibitors, and Connections , 2020, Frontiers in Plant Science.

[19]  Honghe Sun,et al.  Characterization of the OFP Gene Family and its Putative Involvement of Tuberous Root Shape in Radish , 2020, International journal of molecular sciences.

[20]  So Yeon Jeong,et al.  Inhibitory Functions of Novel Compounds from Dioscorea batatas Decne Peel on HMGB1-mediated Septic Responses , 2020, Biotechnology and Bioprocess Engineering.

[21]  Yuehui He,et al.  Roles of Brassinosteroids in Plant Reproduction , 2020, International journal of molecular sciences.

[22]  A. Asfaw,et al.  Review of empirical and emerging breeding methods and tools for yam ( Dioscorea spp.) improvement: Status and prospects , 2019, Plant Breeding.

[23]  K. Malínská,et al.  Brassinosteroid signaling delimits root gravitropism via sorting of the Arabidopsis PIN2 auxin transporter , 2019, Nature Communications.

[24]  Trevor M. Nolan,et al.  Brassinosteroids: Multidimensional Regulators of Plant Growth, Development, and Stress Responses[OPEN] , 2019, Plant Cell.

[25]  C. Rothfels,et al.  Comparative transcriptomics of a monocotyledonous geophyte reveals shared molecular mechanisms of underground storage organ formation , 2019, bioRxiv.

[26]  B. Dijkstra,et al.  β-Xylosidases: Structural Diversity, Catalytic Mechanism, and Inhibition by Monosaccharides , 2019, International journal of molecular sciences.

[27]  D. Xiao,et al.  Integrated mRNA and miRNA transcriptome analysis reveals a regulatory network for tuber expansion in Chinese yam (Dioscorea opposita) , 2019, BMC Genomics.

[28]  Q. Yang,et al.  Identification and Characterization of Brassinosteroid Biosynthesis and Signaling Pathway Genes in Solanum tuberosum , 2019, Russian Journal of Plant Physiology.

[29]  O. Borsani,et al.  TTL Proteins Scaffold Brassinosteroid Signaling Components at the Plasma Membrane to Optimize Signal Transduction in Arabidopsis , 2019, Plant Cell.

[30]  B. Liu,et al.  Brassinosteroid-regulated plant growth and development and gene expression in soybean , 2019, The Crop Journal.

[31]  Xiaolin Ren,et al.  Effects of Brassinosteroid Associated with Auxin and Gibberellin on Apple Tree Growth and Gene Expression Patterns , 2019, Horticultural Plant Journal.

[32]  M. Menossi,et al.  Brassinosteroids, the Sixth Class of Phytohormones: A Molecular View from the Discovery to Hormonal Interactions in Plant Development and Stress Adaptation , 2019, International journal of molecular sciences.

[33]  E. van der Knaap,et al.  Plant Organ Shapes Are Regulated by Protein Interactions and Associations With Microtubules , 2018, Front. Plant Sci..

[34]  E. Knaap,et al.  A common genetic mechanism underlies morphological diversity in fruits and other plant organs , 2018, Nature Communications.

[35]  Jianming Li,et al.  Brassinosteroid Signaling Recruits Histone 3 Lysine-27 Demethylation Activity to FLOWERING LOCUS C Chromatin to Inhibit the Floral Transition in Arabidopsis. , 2018, Molecular plant.

[36]  Tae-Wuk Kim,et al.  Function and molecular regulation of DWARF1 as a C-24 reductase in brassinosteroid biosynthesis in Arabidopsis , 2018, Journal of experimental botany.

[37]  Yansheng Zhang,et al.  Comparative Transcriptome Analysis Identifies Putative Genes Involved in Dioscin Biosynthesis in Dioscorea zingiberensis , 2018, Molecules.

[38]  Qingquan Liu,et al.  Lignins: Biosynthesis and Biological Functions in Plants , 2018, International journal of molecular sciences.

[39]  G. Angenent,et al.  Divergent regulation of Arabidopsis SAUR genes: a focus on the SAUR10-clade , 2017, BMC Plant Biology.

[40]  Yiqing Liu,et al.  Transcriptome analysis reveals the genetic basis underlying the biosynthesis of volatile oil, gingerols, and diarylheptanoids in ginger (Zingiber officinale Rosc.) , 2017, Botanical Studies.

[41]  Chengcai Chu,et al.  Brassinosteroids Regulate OFP1, a DLT Interacting Protein, to Modulate Plant Architecture and Grain Morphology in Rice , 2017, Front. Plant Sci..

[42]  Jie Zhou,et al.  Analysis of Brassinosteroids in Plants , 2017, Journal of Plant Growth Regulation.

[43]  O. Leyser Auxin Signaling1[OPEN] , 2017, Plant Physiology.

[44]  M. Strnad,et al.  Immunoaffinity chromatography combined with tandem mass spectrometry: A new tool for the selective capture and analysis of brassinosteroid plant hormones. , 2017, Talanta.

[45]  Hailing Luo,et al.  Phytohormone Profiling During Tuber Development of Chinese Yam by Ultra-high performance Liquid Chromatography–Triple Quadrupole Tandem Mass Spectrometry , 2017, Journal of Plant Growth Regulation.

[46]  Y. Hang,et al.  Genetic relationship and identification of Dioscorea polystachya cultivars accessed by ISAP and SCAR markers , 2017 .

[47]  Xuefeng Wang,et al.  Transcriptomic profiling of taproot growth and sucrose accumulation in sugar beet (Beta vulgaris L.) at different developmental stages , 2017, PloS one.

[48]  G. Coupland,et al.  PSEUDO RESPONSE REGULATORs stabilize CONSTANS protein to promote flowering in response to day length , 2017, The EMBO journal.

[49]  S. Wendeborn,et al.  Biological activity of brassinosteroids - direct comparison of known and new analogs in planta. , 2017 .

[50]  S. Dutt,et al.  Key players associated with tuberization in potato: potential candidates for genetic engineering , 2017, Critical reviews in biotechnology.

[51]  Langtao Xiao,et al.  Brassinolide Increases Potato Root Growth In Vitro in a Dose-Dependent Way and Alleviates Salinity Stress , 2016, BioMed research international.

[52]  M. Strnad,et al.  The determination of 22 natural brassinosteroids in a minute sample of plant tissue by UHPLC–ESI–MS/MS , 2016, Analytical and Bioanalytical Chemistry.

[53]  Li Xu,et al.  Transcriptome Analysis of Storage Roots and Fibrous Roots of the Traditional Medicinal Herb Callerya speciosa (Champ.) ScHot , 2016, PloS one.

[54]  Jianxiong Li,et al.  OVATE Family Protein 8 Positively Mediates Brassinosteroid Signaling through Interacting with the GSK3-like Kinase in Rice , 2016, PLoS genetics.

[55]  J. Franco-Zorrilla,et al.  Potato StCONSTANS-like1 Suppresses Storage Organ Formation by Directly Activating the FT-like StSP5G Repressor , 2016, Current Biology.

[56]  C. Gowda,et al.  Crops that feed the world 11. Pearl Millet (Pennisetum glaucum L.): an important source of food security, nutrition and health in the arid and semi-arid tropics , 2016, Food Security.

[57]  Wu Jiang,et al.  Characterizing diversity based on nutritional and bioactive compositions of yam germplasm (Dioscorea spp.) commonly cultivated in China , 2016, Journal of food and drug analysis.

[58]  J. Endelman,et al.  Genetic mapping with an inbred line-derived F2 population in potato , 2016, Theoretical and Applied Genetics.

[59]  Karl G. Kugler,et al.  Brassinosteroids Are Master Regulators of Gibberellin Biosynthesis in Arabidopsis , 2015, Plant Cell.

[60]  T. Sakurai,et al.  Genome-wide analysis reveals phytohormone action during cassava storage root initiation , 2015, Plant Molecular Biology.

[61]  L. Duan,et al.  Dynamic transcriptional profiling provides insights into tuberous root development in Rehmannia glutinosa , 2015, Front. Plant Sci..

[62]  N. Nakamichi,et al.  Adaptation to the Local Environment by Modifications of the Photoperiod Response in Crops , 2014, Plant & cell physiology.

[63]  Chao Xie,et al.  Fast and sensitive protein alignment using DIAMOND , 2014, Nature Methods.

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

[65]  Q. Qian,et al.  Brassinosteroid Regulates Cell Elongation by Modulating Gibberellin Metabolism in Rice[C][W][OPEN] , 2014, Plant Cell.

[66]  A. Oshlack,et al.  Corset: enabling differential gene expression analysis for de novo assembled transcriptomes , 2014, Genome Biology.

[67]  M. Sussman,et al.  SAUR Inhibition of PP2C-D Phosphatases Activates Plasma Membrane H+-ATPases to Promote Cell Expansion in Arabidopsis[C][W] , 2014, Plant Cell.

[68]  J. Abelenda,et al.  Flowering and tuberization: a tale of two nightshades. , 2014, Trends in plant science.

[69]  Gynheung An,et al.  Natural variation in OsPRR37 regulates heading date and contributes to rice cultivation at a wide range of latitudes. , 2013, Molecular plant.

[70]  Min Hee Kim,et al.  Identification of Arabidopsis BAK1-associating receptor-like kinase 1 (BARK1) and characterization of its gene expression and brassinosteroid-regulated root phenotypes. , 2013, Plant & cell physiology.

[71]  Xiaohua Wang,et al.  Transcriptome analysis reveals novel genes potentially involved in photoperiodic tuberization in potato. , 2013, Genomics.

[72]  H. Ku,et al.  Molecular phylogeny of Dioscorea(Dioscoreaceae) in East and Southeast Asia , 2013 .

[73]  S. Savaldi-Goldstein,et al.  Brassinosteroids in growth control: how, when and where. , 2013, Plant science : an international journal of experimental plant biology.

[74]  A. Doron-Faigenboim,et al.  Transcriptional profiling of sweetpotato (Ipomoea batatas) roots indicates down-regulation of lignin biosynthesis and up-regulation of starch biosynthesis at an early stage of storage root formation , 2013, BMC Genomics.

[75]  Richard G. F. Visser,et al.  Naturally occurring allele diversity allows potato cultivation in northern latitudes , 2013, Nature.

[76]  Zhi-Yong Wang,et al.  Brassinosteroids regulate organ boundary formation in the shoot apical meristem of Arabidopsis , 2012, Proceedings of the National Academy of Sciences.

[77]  Jia Li,et al.  Regulation of brassinosteroid biosynthesis and inactivation. , 2012, Journal of integrative plant biology.

[78]  M. Tanokura,et al.  Cloning of genes and enzymatic characterizations of novel dioscorin isoforms from Dioscorea japonica. , 2012, Plant science : an international journal of experimental plant biology.

[79]  T. Yokota,et al.  Biosynthesis of a cholesterol-derived brassinosteroid, 28-norcastasterone, in Arabidopsis thaliana , 2011, Journal of experimental botany.

[80]  J. Abelenda,et al.  Control of flowering and storage organ formation in potato by FLOWERING LOCUS T , 2011, Nature.

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

[82]  M. Neff,et al.  Rice CYP734A cytochrome P450s inactivate brassinosteroids in Arabidopsis , 2011, Planta.

[83]  R. Pierik,et al.  Blue-light-mediated shade avoidance requires combined auxin and brassinosteroid action in Arabidopsis seedlings. , 2011, The Plant journal : for cell and molecular biology.

[84]  N. Friedman,et al.  Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data , 2011, Nature Biotechnology.

[85]  Chuan-Yun Li,et al.  KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases , 2011, Nucleic Acids Res..

[86]  Robert D. Finn,et al.  HMMER web server: interactive sequence similarity searching , 2011, Nucleic Acids Res..

[87]  N. Friedman,et al.  Trinity : reconstructing a full-length transcriptome without a genome from RNA-Seq data , 2016 .

[88]  Ana I. Caño-Delgado,et al.  Brassinosteroids control meristem size by promoting cell cycle progression in Arabidopsis roots , 2011, Development.

[89]  Juan A. Oses-Prieto,et al.  PP2A activates brassinosteroid-responsive gene expression and plant growth by dephosphorylating BZR1 , 2010, Nature Cell Biology.

[90]  Hongkai Ji,et al.  Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. , 2010, Developmental cell.

[91]  R. Asiedu,et al.  Crops that feed the World 1. Yams , 2010, Food Security.

[92]  J. Dommes,et al.  Tuber formation and growth of Dioscorea cayenensis-D. rotundata complex: interactions between exogenous and endogenous jasmonic acid and polyamines , 2010, Plant Growth Regulation.

[93]  T. Mizuno,et al.  PSEUDO-RESPONSE REGULATORS 9, 7, and 5 Are Transcriptional Repressors in the Arabidopsis Circadian Clock[W][OA] , 2010, Plant Cell.

[94]  Matthew D. Young,et al.  Gene ontology analysis for RNA-seq: accounting for selection bias , 2010, Genome Biology.

[95]  Ning Ma,et al.  BLAST+: architecture and applications , 2009, BMC Bioinformatics.

[96]  H. Xue,et al.  Genome-wide analysis revealed the complex regulatory network of brassinosteroid effects in photomorphogenesis. , 2009, Molecular plant.

[97]  F. Schröder,et al.  The extracellular EXO protein mediates cell expansion in Arabidopsis leaves , 2009, BMC Plant Biology.

[98]  Hoo Sun Chung,et al.  A Critical Role for the TIFY Motif in Repression of Jasmonate Signaling by a Stabilized Splice Variant of the JASMONATE ZIM-Domain Protein JAZ10 in Arabidopsis[C][W] , 2009, The Plant Cell Online.

[99]  S. Fujioka,et al.  Castasterone is a likely end product of brassinosteroid biosynthetic pathway in rice. , 2008, Biochemical and biophysical research communications.

[100]  W. Kao,et al.  Effects of pH on the total phenolic compound, antioxidative ability and the stability of dioscorin of various yam cultivars , 2008 .

[101]  M. Taniguchi,et al.  Dynamics of Amyloplast Sedimentation in Growing Yam Tubers and Its Possible Role in Graviperception , 2008 .

[102]  J. Micol,et al.  The JAZ family of repressors is the missing link in jasmonate signalling , 2007, Nature.

[103]  T. Mizuno,et al.  Arabidopsis clock-associated pseudo-response regulators PRR9, PRR7 and PRR5 coordinately and positively regulate flowering time through the canonical CONSTANS-dependent photoperiodic pathway. , 2007, Plant & cell physiology.

[104]  Akiyasu C. Yoshizawa,et al.  KAAS: an automatic genome annotation and pathway reconstruction server , 2007, Environmental health perspectives.

[105]  G. An,et al.  Regulation of brassinosteroid responses by phytochrome B in rice. , 2007, Plant, cell & environment.

[106]  D. Sarkar,et al.  Cytokinins antagonize the jasmonates action on the regulation of potato (Solanum tuberosum) tuber formation in vitro , 2006, Plant Cell, Tissue and Organ Culture.

[107]  K. Hibara,et al.  Arabidopsis CUP-SHAPED COTYLEDON3 Regulates Postembryonic Shoot Meristem and Organ Boundary Formation[W] , 2006, The Plant Cell Online.

[108]  D. Gang,et al.  Biosynthesis of curcuminoids and gingerols in turmeric (Curcuma longa) and ginger (Zingiber officinale): identification of curcuminoid synthase and hydroxycinnamoyl-CoA thioesterases. , 2006, Phytochemistry.

[109]  Jianmin Wu,et al.  KOBAS server: a web-based platform for automated annotation and pathway identification , 2006, Nucleic Acids Res..

[110]  Thomas Lengauer,et al.  Improved scoring of functional groups from gene expression data by decorrelating GO graph structure , 2006, Bioinform..

[111]  Harry Smith,et al.  Phytochrome-mediated agravitropism in Arabidopsis hypocotyls requires GIL1 and confers a fitness advantage. , 2006, The Plant journal : for cell and molecular biology.

[112]  P. Craufurd,et al.  Phases of dormancy in Yam tubers (Dioscorea rotundata). , 2006, Annals of botany.

[113]  S. Fujioka,et al.  Arabidopsis CYP90B1 catalyses the early C-22 hydroxylation of C27, C28 and C29 sterols. , 2006, The Plant journal : for cell and molecular biology.

[114]  Ho Bang Kim,et al.  The Regulation of DWARF4 Expression Is Likely a Critical Mechanism in Maintaining the Homeostasis of Bioactive Brassinosteroids in Arabidopsis1 , 2006, Plant Physiology.

[115]  Hoyeun Kim,et al.  Brassinosteroid Signals Control Expression of the AXR3/IAA17 Gene in the Cross-Talk Point with Auxin in Root Development , 2006, Bioscience, biotechnology, and biochemistry.

[116]  M. Chase,et al.  A Plastid Gene Phylogeny of the Yam Genus, Dioscorea: Roots, Fruits and Madagascar , 2005 .

[117]  Juan Miguel García-Gómez,et al.  BIOINFORMATICS APPLICATIONS NOTE Sequence analysis Manipulation of FASTQ data with Galaxy , 2005 .

[118]  S. Yoshida,et al.  Brassinosteroid Homeostasis in Arabidopsis Is Ensured by Feedback Expressions of Multiple Genes Involved in Its Metabolism , 2005, Plant Physiology.

[119]  I. Tiryaki,et al.  The Oxylipin Signal Jasmonic Acid Is Activated by an Enzyme That Conjugates It to Isoleucine in Arabidopsis , 2004, The Plant Cell Online.

[120]  J. B. Reid,et al.  Brassinosteroids Do Not Undergo Long-Distance Transport in Pea. Implications for the Regulation of Endogenous Brassinosteroid Levels1 , 2004, Plant Physiology.

[121]  J. Mazuch,et al.  EXORDIUM regulates brassinosteroid‐responsive genes , 2004, FEBS letters.

[122]  Yukihisa Shimada,et al.  Comprehensive Comparison of Auxin-Regulated and Brassinosteroid-Regulated Genes in Arabidopsis[w] , 2004, Plant Physiology.

[123]  H. Mignouna,et al.  Harnessing modern biotechnology for tropical tuber crop improvement: Yam ( Dioscorea spp.) molecular breeding , 2003 .

[124]  J. Chory,et al.  BRing it on: new insights into the mechanism of brassinosteroid action. , 2003, Journal of experimental botany.

[125]  Z. Hong,et al.  A Rice Brassinosteroid-Deficient Mutant, ebisu dwarf (d2), Is Caused by a Loss of Function of a New Member of Cytochrome P450 Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.014712. , 2003, The Plant Cell Online.

[126]  Christopher L. Main,et al.  Dioscorea oppositifolia L. Phenotypic Evaluations and Comparison of Control Strategies1 , 2003, Weed Technology.

[127]  H. J. Choi,et al.  Bulbil formation and yield responses of Chinese yam to application of gibberellic acid, mepiquat chloride and trinexapac-ethyl , 2003 .

[128]  R. Wattiez,et al.  Effect of jasmonic acid on developmental morphology during in vitro tuberization of Dioscorea alata (L.) , 2003, Plant Growth Regulation.

[129]  J. Biesaga-Kościelniak,et al.  The influence of animal sex hormones on the induction of flowering in Arabidopsis thaliana: comparison with the effect of 24-epibrassinolide , 2003, Plant Cell, Tissue and Organ Culture.

[130]  S. Fujioka,et al.  Organ-Specific Expression of Brassinosteroid-Biosynthetic Genes and Distribution of Endogenous Brassinosteroids in Arabidopsis , 2003, Plant Physiology.

[131]  K. Kanahama,et al.  Interactive Effects of Photoperiods and Plant Growth Regulators on the Development of Tubers and Flowering Spikes in Chinese Yam (Dioscorea opposita) cv. Nagaimo , 2002 .

[132]  Beat Keller,et al.  The Arabidopsis male-sterile mutant dde2-2 is defective in the ALLENE OXIDE SYNTHASE gene encoding one of the key enzymes of the jasmonic acid biosynthesis pathway , 2002, Planta.

[133]  S. Fujioka,et al.  Microarray Analysis of Brassinosteroid-Regulated Genes in Arabidopsis , 2002, Plant Physiology.

[134]  T. Altmann,et al.  Brassinosteroid-Regulated Gene Expression , 2002, Plant Physiology.

[135]  J. Chory,et al.  BES1 Accumulates in the Nucleus in Response to Brassinosteroids to Regulate Gene Expression and Promote Stem Elongation , 2002, Cell.

[136]  J. Chory,et al.  Nuclear-localized BZR1 mediates brassinosteroid-induced growth and feedback suppression of brassinosteroid biosynthesis. , 2002, Developmental cell.

[137]  O. Miersch,et al.  Changes in jasmonate and gibberellin levels during development of potato plants (Solanum tuberosum) , 2002, Plant Growth Regulation.

[138]  M. Chase,et al.  Yams reclassified: a recircumscription of Dioscoreaceae and Dioscoreales , 2002 .

[139]  Thomas D. Schmittgen,et al.  Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. , 2001, Methods.

[140]  Chuan-Hsiao Han,et al.  Antioxidant activities of dioscorin, the storage protein of yam (Dioscorea batatas Decne) tuber. , 2001, Journal of agricultural and food chemistry.

[141]  Hitoshi Onouchi,et al.  CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis , 2001, Nature.

[142]  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.

[143]  P. Craufurd,et al.  DORMANCY IN YAMS , 2001, Experimental Agriculture.

[144]  J. Jásik,et al.  Effects of jasmonic acid and its methylester on in vitro microtuberisation of three food yam (Dioscorea) species , 2000, Plant Cell Reports.

[145]  E. Weiler,et al.  A novel stress-inducible 12-oxophytodienoate reductase from Arabidopsis thaliana provides a potential link between Brassinosteroid-action and Jasmonic-acid synthesis , 2000 .

[146]  S. C. Chang,et al.  Involvement of brassinosteroids in the gravitropic response of primary root of maize. , 2000, Plant physiology.

[147]  J. Chory,et al.  Activation tagging of the floral inducer FT. , 1999, Science.

[148]  W. Hou,et al.  Dioscorins, the major tuber storage proteins of yam (Dioscorea batatas Decne), with dehydroascorbate reductase and monodehydroascorbate reductase activities , 1999 .

[149]  K. Feldmann,et al.  Brassinosteroid-insensitive dwarf mutants of Arabidopsis accumulate brassinosteroids. , 1999, Plant physiology.

[150]  P. Hedden,et al.  Molecular cloning and functional expression of gibberellin 2- oxidases, multifunctional enzymes involved in gibberellin deactivation. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[151]  S. Fujioka,et al.  Activity of brassinosteroids in the dwarf rice lamina inclination bioassay , 1998 .

[152]  D. Vreugdenhil,et al.  The role of gibberellin, abscisic acid, and sucrose in the regulation of potato tuber formation in vitro , 1998, Plant physiology.

[153]  F. Nagy,et al.  Transcription of the Arabidopsis CPD gene, encoding a steroidogenic cytochrome P450, is negatively controlled by brassinosteroids. , 1998, The Plant journal : for cell and molecular biology.

[154]  G. Hagen,et al.  Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. , 1997, The Plant cell.

[155]  J. Chory,et al.  A Putative Leucine-Rich Repeat Receptor Kinase Involved in Brassinosteroid Signal Transduction , 1997, Cell.

[156]  Y. Koda Possible involvement of jasmonates in various morphogenic events , 1997 .

[157]  T. Yokota The structure, biosynthesis and function of brassinosteroids , 1997 .

[158]  C. Douglas Phenylpropanoid metabolism and lignin biosynthesis: from weeds to trees , 1996 .

[159]  F. Lottspeich,et al.  Cloning, molecular and functional characterization of Arabidopsis thaliana allene oxide synthase (CYP 74), the first enzyme of the octadecanoid pathway to jasmonates , 1996, Plant Molecular Biology.

[160]  J. Chory,et al.  A Role for Brassinosteroids in Light-Dependent Development of Arabidopsis , 1996, Science.

[161]  S. Fry,et al.  Arabidopsis TCH4, regulated by hormones and the environment, encodes a xyloglucan endotransglycosylase. , 1995, The Plant cell.

[162]  P. Quail,et al.  Phytochromes: photosensory perception and signal transduction , 1995, Science.

[163]  R. Simon,et al.  The CONSTANS gene of arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors , 1995, Cell.

[164]  P. Oeller,et al.  Early auxin-induced genes encode short-lived nuclear proteins. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[165]  M. Baker,et al.  Physiological and molecular effects of brassinosteroids on Arabidopsis thaliana , 1993, Journal of Plant Growth Regulation.

[166]  A. Pelacho,et al.  Jasmonic Acid induces tuberization of potato stolons cultured in vitro. , 1991, Plant physiology.

[167]  Y. Kikuta,et al.  Possible Involvement of Jasmonic Acid in Tuberization of Yam Plants , 1991 .

[168]  J. Chory,et al.  Phenotypic and Genetic Analysis of det2, a New Mutant That Affects Light-Regulated Seedling Development in Arabidopsis. , 1991, The Plant cell.

[169]  A. Klyosov,et al.  Trends in biochemistry and enzymology of cellulose degradation. , 1990, Biochemistry.

[170]  H. Koshino,et al.  Structure of a Tuber-inducing Stimulus from Potato Leaves (Solanum tuberosum L.) , 1989 .

[171]  G. Lang Dormancy: A New Universal Terminology , 1987, HortScience.

[172]  H. Kindi,et al.  Two Different Pathways Leading to Phenanthrenes and 9,10-Dihydrophenanthrenes of the Genus Dioscorea , 1984 .

[173]  J. C. Díaz Zagoya,et al.  Studies on the regulation of cholesterol metabolism by the use of the structural analogue, diosgenin. , 1971, Biochemical pharmacology.

[174]  J. Lawton The development of the tuber in seedlings of five species of Dioscorea from Nigeria , 1969 .

[175]  D. Coursey Yam storage—I: A review of yam storage practices and of information on storage losses , 1967 .

[176]  F. W. Martin,et al.  Chromosome Numbers and Behavior in Some Species of Dioscorea , 1963 .

[177]  G. Ahammed,et al.  Brassinosteroids' regulation of plant architecture , 2022, Brassinosteroids in Plant Developmental Biology and Stress Tolerance.

[178]  Dong‐Jin Lee,et al.  An introduction to brassinosteroids , 2022, Brassinosteroids in Plant Developmental Biology and Stress Tolerance.

[179]  R. Terauchi,et al.  Population Genomics of Yams: Evolution and Domestication of Dioscorea Species , 2021, Population Genomics.

[180]  U. Eggli,et al.  Dioscoreaceae , 2019, Monocotyledons.

[181]  D. González Plant transcription factors : evolutionary, structural and functional aspects , 2016 .

[182]  P. Laufs,et al.  CUC Transcription Factors: To the Meristem and Beyond , 2016 .

[183]  P. Reddy Tropical Root and Tuber Crops: An Overview , 2015 .

[184]  H. Iwata,et al.  Intra-Specific Ploidy Variations in Cultivated Chinese Yam (Dioscorea polystachya Turcz.) , 2013 .

[185]  Filip Vandenbussche,et al.  Brassinosteroid control of shoot gravitropism interacts with ethylene and depends on auxin signaling components. , 2013, American journal of botany.

[186]  Han Yong Lee,et al.  Overexpression of jasmonic acid carboxyl methyltransferase increases tuber yield and size in transgenic potato , 2010, Plant Biotechnology Reports.

[187]  I. Onwueme Tuber Physiology in Yams (Dioscorea Spp) and its Agricultural Implications* , 2009 .

[188]  S. K. Kim,et al.  Exogenous effect of gibberellins and jasmonate on tuber enlargement of Dioscorea opposita , 2005 .

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

[190]  D. Boulter,et al.  Isolation and characterization of the storage protein of yam tubers (Dioscorea rotundata) , 1983 .

[191]  D. Coursey Tropical Crop. (Book Reviews: Yams. An Account of the Nature, Origins, Cultivation and Utilisation of the Useful Members of the Dioscoreaceae) , 1967 .