HB21/40/53 promote inflorescence arrest through ABA accumulation at the end of flowering

Flowers are produced by the activity of the inflorescence meristem after the floral transition. In plants with indeterminate inflorescences, as Arabidopsis, the final number of flowers produced by the inflorescence meristem will depend on two main factors, the rate of flower production by the meristem and the duration of the phase of inflorescence meristem activity. The end of flowering, understood as the moment when the inflorescence stops the production of new flowers, is associated with the meristem proliferative arrest. At this time point, the meristem ceases to initiate new floral primordia and the unpollinated flowers already formed arrest their development. It has been known for a long time that fruit/seed production induces inflorescence meristem arrest, but the mechanisms controlling this process were elusive. During the last years, the regulation of the end of flowering has started to be elucidated in Arabidopsis. The meristem arrest at the end of flowering is controlled at the genetic level by the FRUITFULL-APETALA2 (FUL-AP2) pathway, that modulates meristem activity. The meristem arrest has been also shown to be controlled at the hormonal level. It has been proposed that auxin could mediate the fruit/seed effect to the meristem. Cytokinins regulation and response have been also proposed as important factors controlling the meristem activity at the end of flowering. Finally, it has been also described that arrested meristems at the end of flowering resembles dormant meristem at the transcriptomic level. Previously, we have shown that the FUL-AP2 pathway controls the expression of the homeodomain leucine zipper transcription factor HOMEOBOX PROTEIN 21 (HB21), a gene involved in the establishment of bud axillary dormancy. In this work we characterize the role of HB21 in the control of the proliferative arrest associated with the end of flowering. We observed that HB21, together with HB40 and HB53, accumulate in the inflorescence apexes at the end of flowering promoting the cessation of inflorescence meristem activity. We also show that HB21 induction of in young apexes is sufficient to induce flower and meristem arrest, likely mediated by an increase in ABA responses. Thus, our work confirms the parallelism proposed between dormant meristems and the arrested meristem at the end of flowering, which appear to be regulated by common pathways, and propose ABA as a new regulator in the control of inflorescence meristem arrest.

[1]  Tom Bennett,et al.  FLOWERING LOCUS T mediates photo-thermal timing of inflorescence meristem arrest in Arabidopsis thaliana , 2023, Plant Physiology.

[2]  Toshiro Ito,et al.  Arrest, Senescence, and Death of Shoot Apical Stem Cells in Arabidopsis thaliana. , 2022, Plant and Cell Physiology.

[3]  K. Ljung,et al.  Cytokinin signaling regulates two-stage inflorescence arrest in Arabidopsis , 2022, bioRxiv.

[4]  C. Ferrándiz,et al.  A cellular analysis of meristem activity at the end of flowering points to cytokinin as a major regulator of proliferative arrest in Arabidopsis , 2021, Current Biology.

[5]  P. Cerdán,et al.  Regulation of Flowering Time: When and Where? , 2021, Current opinion in plant biology.

[6]  M. Goetz,et al.  The role of auxin and sugar signaling in dominance inhibition of inflorescence growth by fruit load , 2021, bioRxiv.

[7]  M. Alves-Ferreira,et al.  Identification of Players Controlling Meristem Arrest Downstream of the FRUITFULL-APETALA2 Pathway. , 2020, Plant physiology.

[8]  Tom Bennett,et al.  Bloom and bust: understanding the nature and regulation of the end of flowering. , 2020, Current opinion in plant biology.

[9]  K. Ljung,et al.  Auxin export from proximal fruits drives arrest in temporally competent inflorescences , 2020, Nature Plants.

[10]  Atsuko Kinoshita,et al.  Genetic and molecular basis of floral induction in Arabidopsis thaliana , 2020, Journal of experimental botany.

[11]  Shusei Sato,et al.  Inflorescence Meristem Fate Is Dependent on Seed Development and FRUITFULL in Arabidopsis thaliana , 2019, Front. Plant Sci..

[12]  K. Kaufmann,et al.  Genetic control of meristem arrest and life span in Arabidopsis by a FRUITFULL-APETALA2 pathway , 2018, Nature Communications.

[13]  X. Zhang,et al.  Type-B ARABIDOPSIS RESPONSE REGULATORs Specify the Shoot Stem Cell Niche by Dual Regulation of WUSCHEL[OPEN] , 2017, The Plant Cell.

[14]  T. Schmülling,et al.  Gain-of-Function Mutants of the Cytokinin Receptors AHK2 and AHK3 Regulate Plant Organ Size, Flowering Time and Plant Longevity1 , 2017, Plant Physiology.

[15]  Pilar Cubas,et al.  Abscisic acid signaling is controlled by a BRANCHED1/HD-ZIP I cascade in Arabidopsis axillary buds , 2016, Proceedings of the National Academy of Sciences.

[16]  Xuecheng Wang,et al.  Egg cell-specific promoter-controlled CRISPR/Cas9 efficiently generates homozygous mutants for multiple target genes in Arabidopsis in a single generation , 2015, Genome Biology.

[17]  S. Finlayson,et al.  Abscisic Acid Is a General Negative Regulator of Arabidopsis Axillary Bud Growth1[OPEN] , 2015, Plant Physiology.

[18]  C. Jung,et al.  Flowering time regulation in crops—what did we learn from Arabidopsis? , 2015, Current opinion in biotechnology.

[19]  J. Kieber,et al.  Cytokinin and the cell cycle. , 2014, Current opinion in plant biology.

[20]  Hong Ma,et al.  Flower Development under Drought Stress: Morphological and Transcriptomic Analyses Reveal Acute Responses and Long-Term Acclimation in Arabidopsis[C][W] , 2013, Plant Cell.

[21]  Srinidhi V. Holalu,et al.  Abscisic Acid Regulates Axillary Bud Outgrowth Responses to the Ratio of Red to Far-Red Light1[C][W][OPEN] , 2013, Plant Physiology.

[22]  J. Kieber,et al.  SCFKMD controls cytokinin signaling by regulating the degradation of type-B response regulators , 2013, Proceedings of the National Academy of Sciences.

[23]  Nese Sreenivasulu,et al.  Contrapuntal role of ABA: does it mediate stress tolerance or plant growth retardation under long-term drought stress? , 2012, Gene.

[24]  G. Coupland,et al.  The genetic basis of flowering responses to seasonal cues , 2012, Nature Reviews Genetics.

[25]  Tanya Z. Berardini,et al.  The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools , 2011, Nucleic Acids Res..

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

[27]  K. Shinozaki,et al.  Analysis of Cytokinin Mutants and Regulation of Cytokinin Metabolic Genes Reveals Important Regulatory Roles of Cytokinins in Drought, Salt and Abscisic Acid Responses, and Abscisic Acid Biosynthesis[C][W] , 2011, Plant Cell.

[28]  T. Schmülling,et al.  Cytokinin Regulates the Activity of Reproductive Meristems, Flower Organ Size, Ovule Formation, and Thus Seed Yield in Arabidopsis thaliana[C][W][OA] , 2011, Plant Cell.

[29]  Xuemei Chen,et al.  Orchestration of the Floral Transition and Floral Development in Arabidopsis by the Bifunctional Transcription Factor APETALA2[W][OA] , 2010, Plant Cell.

[30]  Cole Trapnell,et al.  Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. , 2010, Nature biotechnology.

[31]  T. Kuromori,et al.  ABC transporter AtABCG25 is involved in abscisic acid transport and responses , 2010, Proceedings of the National Academy of Sciences.

[32]  Lior Pachter,et al.  Sequence Analysis , 2020, Definitions.

[33]  Cole Trapnell,et al.  Ultrafast and memory-efficient alignment of short DNA sequences to the human genome , 2009, Genome Biology.

[34]  D. Todorova,et al.  Response of cytokinin pool and cytokinin oxidase/dehydrogenase activity to abscisic acid exhibits organ specificity in peas , 2008, Acta Physiologiae Plantarum.

[35]  Xuemei Chen,et al.  miR172 regulates stem cell fate and defines the inner boundary of APETALA3 and PISTILLATA expression domain in Arabidopsis floral meristems. , 2007, The Plant journal : for cell and molecular biology.

[36]  S. Kurup,et al.  Transactivated and chemically inducible gene expression in plants. , 2006, The Plant journal : for cell and molecular biology.

[37]  Martin Kuiper,et al.  BiNGO: a Cytoscape plugin to assess overrepresentation of Gene Ontology categories in Biological Networks , 2005, Bioinform..

[38]  P. Shannon,et al.  Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks , 2003 .

[39]  K. Cline,et al.  Molecular characterization of the Arabidopsis 9-cis epoxycarotenoid dioxygenase gene family. , 2003, The Plant journal : for cell and molecular biology.

[40]  Imre,et al.  REGIA, An EU Project on Functional Genomics of Transcription Factors From Arabidopsis Thaliana , 2002, Comparative and functional genomics.

[41]  K. Shinozaki,et al.  Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis. , 2001, The Plant journal : for cell and molecular biology.

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

[43]  K. Shinozaki,et al.  Role of arabidopsis MYC and MYB homologs in drought- and abscisic acid-regulated gene expression. , 1997, The Plant cell.

[44]  A. Bleecker,et al.  The Fate of Inflorescence Meristems Is Controlled by Developing Fruits in Arabidopsis , 1994, Plant physiology.

[45]  G. Jürgens,et al.  The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. , 1996, Development.