Early inflorescence development in the grasses (Poaceae)

The shoot apical meristem of grasses produces the primary branches of the inflorescence, controlling inflorescence architecture and hence seed production. Whereas leaves are produced in a distichous pattern, with the primordia separated from each other by an angle of 180°, inflorescence branches are produced in a spiral in most species. The morphology and developmental genetics of the shift in phyllotaxis have been studied extensively in maize and rice. However, in wheat, Brachypodium, and oats, all in the grass subfamily Pooideae, the change in phyllotaxis does not occur; primary inflorescence branches are produced distichously. It is unknown whether the distichous inflorescence originated at the base of Pooideae, or whether it appeared several times independently. In this study, we show that Brachyelytrum, the genus sister to all other Pooideae has spiral phyllotaxis in the inflorescence, but that in the remaining 3000+ species of Pooideae, the phyllotaxis is two-ranked. These two-ranked inflorescences are not perfectly symmetrical, and have a clear “front” and “back;” this developmental axis has never been described in the literature and it is unclear what establishes its polarity. Strictly distichous inflorescences appear somewhat later in the evolution of the subfamily. Two-ranked inflorescences also appear in a few grass outgroups and sporadically elsewhere in the family, but unlike in Pooideae do not generally correlate with a major radiation of species. After production of branches, the inflorescence meristem may be converted to a spikelet meristem or may simply abort; this developmental decision appears to be independent of the branching pattern.

[1]  A. Vegetti,et al.  Macroevolution of panicoid inflorescences: a history of contingency and order of trait acquisition. , 2013, Annals of botany.

[2]  D. Sokoloff,et al.  Racemose inflorescences of monocots: structural and morphogenetic interaction at the flower/inflorescence level. , 2013, Annals of botany.

[3]  P. Prusinkiewicz,et al.  The interplay between inflorescence development and function as the crucible of architectural diversity. , 2013, Annals of botany.

[4]  D. Jackson,et al.  Quantitative variation in maize kernel row number is controlled by the FASCIATED EAR2 locus , 2013, Nature Genetics.

[5]  V. B. Youngner,et al.  The Biology and Utilization of Grasses , 2012 .

[6]  P. Rudall,et al.  Morphological evolution in the graminid clade: comparative floral anatomy of the grass relatives Flagellariaceae and Joinvilleaceae , 2012 .

[7]  P. Rudall,et al.  Homologies of the flower and inflorescence in the early-divergent grass Anomochloa (Poaceae). , 2012, American journal of botany.

[8]  M. Nei,et al.  MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. , 2011, Molecular biology and evolution.

[9]  Dennis W. Stevenson,et al.  Assembling the Tree of the Monocotyledons: Plastome Sequence Phylogeny and Evolution of Poales1 , 2010 .

[10]  M. A. Patrick,et al.  The aerodynamics and efficiency of wind pollination in grasses , 2010 .

[11]  C. Baskin,et al.  Effect of seed position in spikelet on life history of Eremopyrum distans (Poaceae) from the cold desert of north-west China. , 2010, Annals of botany.

[12]  D. Salariato,et al.  Molecular phylogeny of the subtribe Melinidinae (Poaceae: Panicoideae: Paniceae) and evolutionary trends in the homogenization of inflorescences. , 2010, Molecular phylogenetics and evolution.

[13]  P. K. Endress Disentangling confusions in inflorescence morphology: Patterns and diversity of reproductive shoot ramification in angiosperms , 2010 .

[14]  M. Barton,et al.  Twenty years on: the inner workings of the shoot apical meristem, a developmental dynamo. , 2010, Developmental biology.

[15]  Sarah Hake,et al.  The maize SBP-box transcription factor encoded by tasselsheath4 regulates bract development and the establishment of meristem boundaries , 2010, Development.

[16]  F. Taguchi-Shiobara,et al.  A Conserved Mechanism of Bract Suppression in the Grass Family[W][OA] , 2010, Plant Cell.

[17]  T. Hirose,et al.  A gene controlling the number of primary rachis branches also controls the vascular bundle formation and hence is responsible to increase the harvest index and grain yield in rice , 2010, Theoretical and Applied Genetics.

[18]  Stephen A. Smith,et al.  Phylogenetic analyses reveal the shady history of C4 grasses , 2010, Proceedings of the National Academy of Sciences.

[19]  Jiansheng Liang,et al.  ERECT PANICLE2 Encodes a Novel Protein That Regulates Panicle Erectness in Indica Rice , 2010, Genetics.

[20]  D. Sokoloff,et al.  Morphology and development of the gynoecium in Centrolepidaceae: The most remarkable range of variation in Poales. , 2009, American journal of botany.

[21]  G. An,et al.  Map-based cloning of the ERECT PANICLE 3 gene in rice , 2009, Theoretical and Applied Genetics.

[22]  E. Kellogg,et al.  MADS-box gene expression and implications for developmental origins of the grass spikelet. , 2009, American journal of botany.

[23]  S. Iida,et al.  Expression Level of ABERRANT PANICLE ORGANIZATION1 Determines Rice Inflorescence Form through Control of Cell Proliferation in the Meristem1[W] , 2009, Plant Physiology.

[24]  A. Vegetti,et al.  Diversification of inflorescence development in the PCK clade (Poaceae: Panicoideae: Paniceae). , 2009, American journal of botany.

[25]  P. Rudall,et al.  Reproductive morphology of the early-divergent grass Streptochaeta and its bearing on the homologies of the grass spikelet , 2008, Plant Systematics and Evolution.

[26]  M. Sundberg,et al.  Phyllotactic pattern is altered in the transition to flowering in the early ears of Zea mays landrace chapalote (Poaceae). , 2008, American journal of botany.

[27]  Mattijs Bliek,et al.  Patterning of Inflorescences and Flowers by the F-Box Protein DOUBLE TOP and the LEAFY Homolog ABERRANT LEAF AND FLOWER of Petunia[W] , 2008, The Plant Cell Online.

[28]  Queenie K.-G. Tan,et al.  An Arabidopsis F-box protein acts as a transcriptional co-factor to regulate floral development , 2008, Development.

[29]  P. Catalán,et al.  Phylogeny of the tribe Aveneae (Pooideae, Poaceae) inferred from plastid trnT-F and nuclear ITS sequences. , 2007, American journal of botany.

[30]  J. Kyozuka,et al.  Rice ABERRANT PANICLE ORGANIZATION 1, encoding an F-box protein, regulates meristem fate. , 2007, The Plant journal : for cell and molecular biology.

[31]  Dianxiang Zhang,et al.  Inflorescence diversification in the "finger millet clade" (Chloridoideae, Poaceae): a comparison of molecular phylogeny and developmental morphology. , 2007, American journal of botany.

[32]  P. Prusinkiewicz,et al.  Evolution and Development of Inflorescence Architectures , 2007, Science.

[33]  P. Rudall,et al.  Floral Development and Embryology in the Early‐Divergent Grass Pharus , 2007, International Journal of Plant Sciences.

[34]  M. Zanis,et al.  Conservation of B class gene expression in the second whorl of a basal grass and outgroups links the origin of lodicules and petals , 2007, Proceedings of the National Academy of Sciences.

[35]  H. Kitano,et al.  Conservation and diversification of meristem maintenance mechanism in Oryza sativa: Function of the FLORAL ORGAN NUMBER2 gene. , 2006, Plant & cell physiology.

[36]  Hong Ma,et al.  The FLORAL ORGAN NUMBER4 Gene Encoding a Putative Ortholog of Arabidopsis CLAVATA3 Regulates Apical Meristem Size in Rice1[W] , 2006, Plant Physiology.

[37]  S. Kresovich,et al.  Inheritance of inflorescence architecture in sorghum , 2006, Theoretical and Applied Genetics.

[38]  G. Haughn,et al.  UFO in the Arabidopsis inflorescence apex is required for floral-meristem identity and bract suppression , 2006, Planta.

[39]  K. Jung,et al.  The rice FON1 gene controls vegetative and reproductive development by regulating shoot apical meristem size. , 2006, Molecules and cells.

[40]  L. Harder,et al.  Functional associations of floret and inflorescence traits among grass species. , 2005, American journal of botany.

[41]  B. G. Briggs,et al.  Evolution of reproductive structures in grasses (Poaceae) inferred by sister-group comparison with their putative closest living relatives, Ecdeiocoleaceae. , 2005, American journal of botany.

[42]  Y. Nagato,et al.  ABERRANT PANICLE ORGANIZATION 1 temporally regulates meristem identity in rice. , 2005, Developmental biology.

[43]  A. Doust,et al.  A Naked Grass in the “Bristle Clade”: A Phylogenetic and Developmental Study of Panicum Section Bulbosa (Paniceae: Poaceae) , 2005, International Journal of Plant Sciences.

[44]  A. Vegetti,et al.  Inflorescence, spikelet, and floral development in Panicum maximum and Urochloa plantaginea (Poaceae). , 2005, American journal of botany.

[45]  S. Hake,et al.  thick tassel dwarf1 encodes a putative maize ortholog of the Arabidopsis CLAVATA1 leucine-rich repeat receptor-like kinase , 2005, Development.

[46]  D. Jackson,et al.  Genetics and evolution of inflorescence and flower development in grasses. , 2005, Plant & cell physiology.

[47]  L. Harder,et al.  Inflorescence architecture and wind pollination in six grass species , 2004 .

[48]  Makoto Sato,et al.  The gene FLORAL ORGAN NUMBER1 regulates floral meristem size in rice and encodes a leucine-rich repeat receptor kinase orthologous to Arabidopsis CLAVATA1 , 2004, Development.

[49]  A. Doust,et al.  Taxonomy, Phylogeny, and Inflorescence Development of the Genus Ixophorus (Panicoideae: Poaceae) , 2004, International Journal of Plant Sciences.

[50]  Elizabeth A Kellogg,et al.  The evolution of nuclear genome structure in seed plants. , 2004, American journal of botany.

[51]  Caz M Taylor,et al.  Pollen limitation causes an Allee effect in a wind-pollinated invasive grass (Spartina alterniflora). , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[52]  D. Jackson,et al.  Control of phyllotaxy by the cytokinin-inducible response regulator homologue ABPHYL1 , 2004, Nature.

[53]  M. Tuda,et al.  A New Species Megabruchidius sophorae (Coleoptera, Bruchidae), Feeding on Seeds of Styphnolobium (Fabaceae) New to Bruchidae , 2004, Zoological science.

[54]  G. Muehlbauer,et al.  Genetic and morphological characterization of the barley uniculm2 (cul2) mutant , 2003, Theoretical and Applied Genetics.

[55]  J. Stougaard,et al.  Proliferating Floral Organs (Pfo), a Lotus japonicus gene required for specifying floral meristem determinacy and organ identity, encodes an F-box protein. , 2003, The Plant journal : for cell and molecular biology.

[56]  A. Doust,et al.  Inflorescence diversification in the panicoid "bristle grass" clade (Paniceae, Poaceae): evidence from molecular phylogenies and developmental morphology. , 2002, American journal of botany.

[57]  A. Doust The Developmental Basis of Floral Variation in Drimys winteri (Winteraceae) , 2001, International Journal of Plant Sciences.

[58]  J. Hofer,et al.  Stamina pistilloida, the Pea Ortholog of Fim and UFO, Is Required for Normal Development of Flowers, Inflorescences, and Leaves , 2001, Plant Cell.

[59]  E. Kellogg,et al.  Floral development and the formation of unisexual spikelets in the Andropogoneae (Poaceae). , 1999, American journal of botany.

[60]  S. Hake,et al.  Control of phyllotaxy in maize by the abphyl1 gene. , 1999, Development.

[61]  R. Reuter,et al.  Formation of Panicles and Hermaphroditic Florets in Wild-Rice , 1998, International Journal of Plant Sciences.

[62]  M. McKone,et al.  Reproductive biology of two dominant prairie grasses (Andropogon gerardii and Sorghastrum nutans, Poaceae): male-biased sex allocation in wind-pollinated plants? , 1998, American journal of botany.

[63]  S. Briggs,et al.  Regulation of leaf initiation by the terminal ear 1 gene of maize , 1998, Nature.

[64]  F. Weberling,et al.  The structure of the paracladial zone in Poaceae , 1996 .

[65]  G. Rua,et al.  The inflorescences of Digitaria phaeotrix: morphological and developmental aspects. , 1996 .

[66]  S. Lubkin Phyllotaxis: A systemic study in plant morphogenesis , 1995 .

[67]  L. Trabaud,et al.  Effects of high temperatures, ash and seed position in the inflorescence on the germination of three Spanish grasses , 1994 .

[68]  R. V. Jean,et al.  Phyllotaxis: A Systemic Study in Plant Morphogenesis , 1995 .

[69]  R. Pharis,et al.  Early panicle development in Chionochloa macra plants induced to flower by 2,2 dimethyl gibberellin A4 or long days , 1993 .

[70]  E. Kokko,et al.  Panicle, spikelet, and floret development in orchardgrass (Dactylis glomerata) , 1993 .

[71]  G. M. Simpson Seed Dormancy in Grasses , 1990 .

[72]  J. Porter,et al.  Development of the Inflorescence in Wild Oats , 1990 .

[73]  W. Stür Reproductive development of the apex of Brachiaria decumbens Stapf , 1986 .

[74]  R. Schmid,et al.  Floral initiation in field crops. An atlas of scanning electron micrographs. , 1982 .

[75]  H. M. Dale,et al.  A DEVELOPMENTAL STUDY OF WILD RICE, ZIZANIA AQUATICA L. , 1960 .

[76]  B. Sharman Leaf and Bud Initiation in the Gramineae , 1945, Botanical Gazette.

[77]  T. Hodkinson,et al.  New grass phylogeny resolves deep evolutionary relationships and discovers C4 origins. , 2012, The New phytologist.

[78]  By O. T. Bonnett THE DEVELOPMENT OF THE WHEAT SPIKE ^ , 2010 .

[79]  R. Soreng,et al.  Phylogenetics of the Grass _Aveneae-Type Plastid DNA Clade_ (Poaceae: Pooideae, Poeae) Based on Plastid and Nuclear Ribosomal DNA Sequence Data , 2010 .

[80]  D. Sokoloff,et al.  A new species of Centrolepis (Centrolepidaceae, Poales) from Northern Australia, with remarkable inflorescence architecture. , 2009 .

[81]  D. Maddison,et al.  Mesquite: a modular system for evolutionary analysis. Version 2.6 , 2009 .

[82]  Jerrold I. Davis,et al.  Phylogenetic relationships among Poaceae and related families as inferred from morphology, inversions in the plastid genome, and sequence data from the mitochondrial and plastid genomes. , 2003, American journal of botany.

[83]  C. Vegetti,et al.  The grass inflorescence , 1998 .

[84]  武岡 洋治,et al.  Scanning electron microscopic observations on morphogenesis of the panicle and spikelet in rice plants. , 1989 .

[85]  T. Soderstrom,et al.  Morphological, Anatomical, and Taxonomic Studies in Anomochloa and Streptochaeta (Poaceae: Bambusoideae) , 1988 .

[86]  L. Dillon The Gene , 1987, Springer US.

[87]  A. Lawson,et al.  New Species , 1897, Botanical Gazette.

[88]  O. T. Bonnett Development of the staminate and pistillate inflorescences of sweet corn. , 1940 .

[89]  M. W. Evans,et al.  Developmental morphology of the growing point of the shoot and the inflorescence in grasses. , 1940 .