Barren Inflorescence2 Encodes A Co-Ortholog Of The PINOID Serine/Threonine Kinase And Is Required For Organogenesis During Inflorescence And Vegetative Development In Maize1[C][W][OA]
P. McSteen, S. Malcomber, A. Skirpan, C. Lunde, Xianting Wu, E. Kellogg, S. Hake
Published 2007 · Biology, Medicine
Download PDFAnalyze on Scholarcy
Organogenesis in plants is controlled by meristems. Axillary meristems, which give rise to branches and flowers, play a critical role in plant architecture and reproduction. Maize (Zea mays) and rice (Oryza sativa) have additional types of axillary meristems in the inflorescence compared to Arabidopsis (Arabidopsis thaliana) and thus provide an excellent model system to study axillary meristem initiation. Previously, we characterized the barren inflorescence2 (bif2) mutant in maize and showed that bif2 plays a key role in axillary meristem and lateral primordia initiation in the inflorescence. In this article, we cloned bif2 by transposon tagging. Isolation of bif2-like genes from seven other grasses, along with phylogenetic analysis, showed that bif2 is a co-ortholog of PINOID (PID), which regulates auxin transport in Arabidopsis. Expression analysis showed that bif2 is expressed in all axillary meristems and lateral primordia during inflorescence and vegetative development in maize and rice. Further phenotypic analysis of bif2 mutants in maize illustrates additional roles of bif2 during vegetative development. We propose that bif2/PID sequence and expression are conserved between grasses and Arabidopsis, attesting to the important role they play in development. We provide further support that bif2, and by analogy PID, is required for initiation of both axillary meristems and lateral primordia.
This paper references
P. McSteen (2005)
The maize mutant barren stalk1 is defective in axillary meristem development.
Matthew K. Ritter (2002)
Heterogeneous Expression Patterns and Separate Roles of the SEPALLATA Gene LEAFY HULL STERILE1 in Grasses
S. Malcomber (2004)
The LAX1 and FRIZZY PANICLE 2 genes determine the inflorescence architecture of rice by controlling rachis-branch and spikelet development.
M. Komatsu (2001)
D. Lisch (2002)
The Genomes of Oryza sativa: A History of Duplications
J. Yu (2005)
MacClade 4: analysis of phy-logeny and character evolution
D. Maddison (2003)
The PINOID protein kinase regulates organ development in Arabidopsis by enhancing polar auxin transport.
R. Benjamins (2001)
Regulation of phyllotaxis by polar auxin transport
D. Reinhardt (2003)
Structural and Functional Insights into the Regulation of Arabidopsis AGC VIIIa Kinases*
H. Zegzouti (2006)
The Mu elements of Zea mays.
V. Chandler (1992)
Shoot and inflorescence branching.
G. Schmitz (2005)
A PINOID-Dependent Binary Switch in Apical-Basal PIN Polar Targeting Directs Auxin Efflux
J. Friml (2004)
Expression of maize KNOTTED1 related homeobox genes in the shoot apical meristem predicts patterns of morphogenesis in the vegetative shoot
D. Jackson (1994)
Organ initiation and the development of unisexual flowers in the tassel and ear of zea mays
P. Cheng (1983)
The Impact of the Species–Area Relationship on Estimates of Paleodiversity
Anthony D. Barnosky (2005)
Morphogenesis in pinoid mutants of Arabidopsis thaliana
Sally R. M. Bennett (1995)
Control of tillering in rice
Xueyong Li (2003)
Phosphorylation and activation of PINOID by the phospholipid signaling kinase 3-phosphoinositide-dependent protein kinase 1 (PDK1) in Arabidopsis.
H. Zegzouti (2006)
Suppressor of sessile spikelets1 (Sosl): a dominant mutant affecting inflorescence development in maize
J. Doebley (1995)
Urea-based Plant DNA Miniprep
J. Chen (1994)
The evolution of apical dominance in maize
J. Doebley (1997)
Patterns in Plant Development
T. A. Steeves (1974)
MRBAYES: Bayesian inference of phylogenetic trees
J. Huelsenbeck (2001)
The protein kinase family: conserved features and deduced phylogeny of the catalytic domains.
S. Hanks (1988)
FRIZZY PANICLE is required to prevent the formation of axillary meristems and to establish floral meristem identity in rice spikelets
M. Komatsu (2003)
The Polar Auxin Transport Inhibitor N-1-Naphthylphthalamic Acid Disrupts Leaf Initiation, KNOX Protein Regulation, and Formation of Leaf Margins in Maize
M. Scanlon (2003)
Class II tassel seed mutations provide evidence for multiple types of inflorescence meristems in maize (Poaceae).
E. Irish (1997)
Molecular characterization and expression of PsPK2, a PINOID-like gene from pea (Pisum sativum)
Fang Bai (2005)
A role for flavin monooxygenase-like enzymes in auxin biosynthesis.
Y. Zhao (2001)
Plant DNA Miniprep and Microprep: Versions 2.1–2.3
S. Dellaporta (1994)
A floret by any other name: control of meristem identity in maize.
P. McSteen (2000)
LAX and SPA: Major regulators of shoot branching in rice
K. Komatsu (2003)
Requirement of the Auxin Polar Transport System in Early Stages of Arabidopsis Floral Bud Formation.
K. Okada (1991)
Gramineae. Flora of Tropical Africa
O Stapf (1917)
Expression patterns and mutant phenotype of teosinte branched1 correlate with growth suppression in maize and teosinte.
L. Hubbard (2002)
Genetic and morphological characterization of the barley uniculm2 (cul2) mutant
S. Babb (2003)
Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis.
Y. Cheng (2006)
Axillary bud outgrowth: sending a message.
C. Beveridge (2006)
The Genetics of Corn
E. H. Coe (1988)
The role of barren stalk1 in the architecture of maize
A. Gallavotti (2004)
PINOID Positively Regulates Auxin Efflux in Arabidopsis Root Hair Cells and Tobacco Cells[W]
S. Lee (2006)
PIN Proteins Perform a Rate-Limiting Function in Cellular Auxin Efflux
J. Petrášek (2006)
thick tassel dwarf1 encodes a putative maize ortholog of the Arabidopsis CLAVATA1 leucine-rich repeat receptor-like kinase
P. Bommert (2005)
Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics.
A. Paterson (2004)
A PIN1 family gene, OsPIN1, involved in auxin-dependent adventitious root emergence and tillering in rice.
Min Xu (2005)
Rice as a model for comparative genomics of plants.
K. Shimamoto (2002)
Developmental Gene Evolution and the Origin of Grass Inflorescence Diversity
S. Malcomber (2006)
Ear and Tassel Development in Maize
O. T. Bonnett (1948)
barren inflorescence2 regulates axillary meristem development in the maize inflorescence.
P. McSteen (2001)
Orthology, paralogy and proposed classification for paralog subtypes.
E. L. Sonnhammer (2002)
Activities of auxin polar transport in inflorescence axes of flower mutants ofArabidopsis thaliana: Relevance to flower formation and growth
M. Oka (2006)
Ectopic expression of rice OsMADS1 reveals a role in specifying the lemma and palea, grass floral organs analogous to sepals
K. Prasad (2001)
ZmPIN1a and ZmPIN1b Encode Two Novel Putative Candidates for Polar Auxin Transport and Plant Architecture Determination of Maize1[W]
Nicola Carraro (2006)
Genetics and evolution of inflorescence and flower development in grasses.
Peter Bommert (2005)
Auxin Regulates the Initiation and Radial Position of Plant Lateral Organs
D. Reinhardt (2000)
The PIN auxin efflux facilitators: evolutionary and functional perspectives.
I. Paponov (2005)
The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development
C. Hardtke (1998)
Growth signalling pathways in Arabidopsis and the AGC protein kinases.
L. Bögre (2003)
Studies on the role of the Arabidopsis gene MONOPTEROS in vascular development and plant cell axialization
G. Przemeck (2004)
Gapped BLAST and PSI-BLAST: A new
D. Lipman (1997)
Regulation of Auxin Response by the Protein Kinase PINOID
S. Christensen (2000)
Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue.
L. Gälweiler (1998)
MODELTEST: testing the model of DNA substitution
D. Posada (1998)
The Maize Handbook
M. Freeling (1994)
Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events
Multiple sequence alignment with ClustalX
F Jeanmougin (1998)
Phyllotaxis--a new chapter in an old tale about beauty and magic numbers.
D. Reinhardt (2005)
Comparative analysis of axillary and floral meristem development
V. Grbic (2005)
The Roles of Auxin Response Factor Domains in Auxin-Responsive Transcription Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.008417.
S. Tiwari (2003)
Initiation of axillary and floral meristems in Arabidopsis.
J. Long (2000)
Spikelet and floral morphology
H T Clifford (1987)
Characterization of OsPID, the rice ortholog of PINOID, and its possible involvement in the control of polar auxin transport.
Y. Morita (2007)
Multiple sequence alignment with Clustal X.
F. Jeanmougin (1998)
The fasciated ear2 gene encodes a leucine-rich repeat receptor-like protein that regulates shoot meristem proliferation in maize.
F. Taguchi-Shiobara (2001)
This paper is referenced by
NEEDLE1 encodes a mitochondria localized ATP-dependent metalloprotease required for thermotolerant maize growth
Qiujie Liu (2019)
The barren stalk2 Gene Is Required for Axillary Meristem Development in Maize.
Hong Yao (2019)
Phosphorylation of Conserved PIN Motifs Directs Arabidopsis PIN1 Polarity and Auxin Transport[W][OA]
F. Huang (2010)
LAX PANICLE2 of Rice Encodes a Novel Nuclear Protein and Regulates the Formation of Axillary Meristems[W]
H. Tabuchi (2011)
Genetic regulation of polar auxin transport and its role in control of shoot morphogenesis
U. N. Kavai-ool (2011)
Mutations in CsPID encoding a Ser/Thr protein kinase are responsible for round leaf shape in cucumber (Cucumis sativus L.)
Chaowen Zhang (2018)
Forward genetic analysis of cellulose biosynthesis inhibitor resistance and wall hydrolysis sensitivity.
Isaac Shim (2014)
Genetic mechanisms of maize development: from gametophyte to flowers
S. Federici (2014)
The DNA binding landscape of the maize AUXIN RESPONSE FACTOR family
M. Galli (2018)
Sporisorium reilianum Infection Changes Inflorescence and Branching Architectures of Maize1[C][W][OA]
H. Ghareeb (2011)
The role of auxin in shaping shoot architecture.
A. Gallavotti (2013)
Developmental disasteri: A novel mutation causing
P. McSteen (2009)
Maize LAZY1 Mediates Shoot Gravitropism and Inflorescence Development through Regulating Auxin Transport, Auxin Signaling, and Light Response1[C][W]
Z. Dong (2013)
Control of maize development by microRNA and auxin regulated pathways
Jessica E. Wilson (2018)
Pleiotropic effects of ZmLAZY1 on the auxin-mediated responses to gravity and light in maize shoot and inflorescences
Z. Dong (2013)
Distinct regulatory role for RFL, the rice LFY homolog, in determining flowering time and plant architecture
Nagashree N. Rao (2008)
Recent advances in auxin research in rice and their implications for crop improvement.
Yidong Wang (2018)
OsPINOID Regulates Stigma and Ovule Initiation through Maintenance of the Floral Meristem by Auxin Signaling1
M. Xu (2019)
The Ha-ROXL gene is required for initiation of axillary and floral meristems in sunflower.
Alice Basile (2019)
Fine mapping and identification of ub4 as a candidate gene associated with tassel branch number in maize (Zea mays L.)
J. Li (2019)
Aberrant spikelet and panicle1, encoding a TOPLESS-related transcriptional co-repressor, is involved in the regulation of meristem fate in rice.
Akiko Yoshida (2012)
Auxin signaling modules regulate maize inflorescence architecture
M. Galli (2015)
Identification of a candidate gene underlying qKRN5b for kernel row number in Zea mays L.
Xiaomeng Shen (2019)
Hormonal control of grass inflorescence development.
Solmaz Barazesh (2008)
Integrated Meta-QTL and Genome-Wide Association Study Analyses Reveal Candidate Genes for Maize Yield
Yijun Wang (2019)
Mutagenesis – the Key to Genetic Analysis
M. Neuffer (2009)
ZmPIN1-Mediated Auxin Transport Is Related to Cellular Differentiation during Maize Embryogenesis and Endosperm Development1[W]
C. Forestan (2009)
Natural variation in maize architecture is mediated by allelic differences at the PINOID co-ortholog barren inflorescence2.
Gael Pressoir (2009)
Identification of quantitative trait locus and epistatic interaction for degenerated spikelets on the top of panicle in rice
C. Tan (2011)
Meristem identity and phyllotaxis in inflorescence development
Madelaine E Bartlett (2014)
Plant Responses and Tolerance to High Temperature Stress: Role of Exogenous Phytoprotectants
Kamrun Nahar (2015)
Sparse panicle1 is required for inflorescence development in Setaria viridis and maize
Pu Huang (2017)See more