Time to Stop: Flower Meristem Termination

Prunet, Nathanaël; Morel, Patrice; Negrutiu, Ioan; Tréhin, Christophe

doi:10.1104/pp.109.141812

Cited by 51 publications

(55 citation statements)

References 89 publications

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“…The small SAM size of fhy3 as a result of the de-repressed CLV3 expression and the reduced WUS expression was paradoxical to the severe FM indeterminacy of fhy3 ag-10 with prolonged WUS expression, which indicates that FHY3 may act through a genetic pathway parallel to the CLV3 pathway in the FM determinacy because the temporal expression of WUS is more important than its relative expression level for FM activity regulation (30). Subsequently, this hypothesis was reinforced by the identification of SEP1 and SEP2 as FHY3 target genes.…”

Section: Discussionmentioning

confidence: 99%

FAR-RED ELONGATED HYPOCOTYL3 activates SEPALLATA2 but inhibits CLAVATA3 to regulate meristem determinacy and maintenance in Arabidopsis

Guo

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Plant meristems are responsible for the generation of all plant tissues and organs. Here we show that the transcription factor (TF) FAR-RED ELONGATED HYPOCOTYL3 (FHY3) plays an important role in both floral meristem (FM) determinacy and shoot apical meristem maintenance in Arabidopsis, in addition to its well-known multifaceted roles in plant growth and development during the vegetative stage. Through genetic analyses, we show that WUSCHEL (WUS) and CLAVATA3 (CLV3), two central players in the establishment and maintenance of meristems, are epistatic to FHY3. Using genome-wide ChIP-seq and RNA-seq data, we identify hundreds of FHY3 target genes in flowers and find that FHY3 mainly acts as a transcriptional repressor in flower development, in contrast to its transcriptional activator role in seedlings. Binding motif-enrichment analyses indicate that FHY3 may coregulate flower development with three flowerspecific MADS-domain TFs and four basic helix-loop-helix TFs that are involved in photomorphogenesis. We further demonstrate that CLV3, SEPALLATA1 (SEP1), and SEP2 are FHY3 target genes. In shoot apical meristem, FHY3 directly represses CLV3, which consequently regulates WUS to maintain the stem cell pool. Intriguingly, CLV3 expression did not change significantly in fhy3 and phytochrome B mutants before and after light treatment, indicating that FHY3 and phytochrome B are involved in light-regulated meristem activity. In FM, FHY3 directly represses CLV3, but activates SEP2, to ultimately promote FM determinacy. Taken together, our results reveal insights into the mechanisms of meristem maintenance and determinacy, and illustrate how the roles of a single TF may vary in different organs and developmental stages. meristem maintenance | meristem determinacy | FHY3 | CLV3 | SEP2 P lant meristems are responsible for the generation of all plant tissues and organs. Unlike the shoot apical meristem (SAM), whose activity is maintained throughout the life of plants, the floral meristem (FM) is precisely programmed to terminate in a process known as FM determinacy (1). WUSCHEL (WUS) plays a central role in the establishment and maintenance of SAM, inflorescence meristem, and FM, as well as in FM determinacy (2-4). WUS is expressed in the organizing center located beneath the stem cells in the meristem to promote cell proliferation by maintaining stem cell potential (2). The WUS/CLAVATA3 (CLV3) signaling pathway maintains the stabilization of meristem size and the stem cell pool (3, 5). Consistent with WUS overactivation, clv3 mutants have an enlarged SAM and increased numbers of floral organs and whorls (5). In addition to the WUS/CLV3 loop, several other pathways are known to regulate FM determinacy (4). AGAMOUS (AG) encodes a MADS-box transcription factor (TF) and is the lynchpin of the FM determinacy network (4, 6, 7). In the null ag-1 mutant, FM determinacy is severely impaired, resulting in a flower-in-flower phenotype (6). AG inhibits WUS expression through both indirect and direct means (8, 9). A number of other gene...

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Section: Discussionmentioning

confidence: 99%

FAR-RED ELONGATED HYPOCOTYL3 activates SEPALLATA2 but inhibits CLAVATA3 to regulate meristem determinacy and maintenance in Arabidopsis

Guo

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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“…Floral organs are formed by a floral meristem, a pool of pluripotent and dividing cells (Prunet et al, 2009). The regulation of the floral meristem seems to be widely conserved among angiosperms (Ferrario et al, 2004;Prunet et al, 2009).…”

Section: Regulation Of Rice Floral Meristem Terminationmentioning

confidence: 99%

“…The regulation of the floral meristem seems to be widely conserved among angiosperms (Ferrario et al, 2004;Prunet et al, 2009). In Arabidopsis, AG is a master regulator terminating the floral meristem by turning WUSCHEL (WUS) off (Sieburth et al, 1998;Sun et al, 2009).…”

Section: Regulation Of Rice Floral Meristem Terminationmentioning

confidence: 99%

Genetic Interaction ofOsMADS3,DROOPING LEAF, andOsMADS13in Specifying Rice Floral Organ Identities and Meristem Determinacy

Liang

Yin

et al. 2011

Plant Physiology

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Grass plants develop unique floral patterns that determine grain production. However, the molecular mechanism underlying the specification of floral organ identities and meristem determinacy, including the interaction among floral homeotic genes, remains largely unknown in grasses. Here, we report the interactions of rice (Oryza sativa) floral homeotic genes, OsMADS3 (a C-class gene), OsMADS13 (a D-class gene), and DROOPING LEAF (DL), in specifying floral organ identities and floral meristem determinacy. The interaction among these genes was revealed through the analysis of double mutants. osmads13-3 osmads3-4 displayed a loss of floral meristem determinacy and generated abundant carpelloid structures containing severe defective ovules in the flower center, which were not detectable in the single mutant. In addition, in situ hybridization and yeast two-hybrid analyses revealed that OsMADS13 and OsMADS3 did not regulate each other's transcription or interact at the protein level. This indicates that OsMADS3 plays a synergistic role with OsMADS13 in both ovule development and floral meristem termination. Strikingly, osmads3-4 dl-sup6 displayed a severe loss of floral meristem determinacy and produced supernumerary whorls of lodicule-like organs at the forth whorl, suggesting that OsMADS3 and DL synergistically terminate the floral meristem. Furthermore, the defects of osmads13-3 dl-sup6 flowers appeared identical to those of dl-sup6, and the OsMADS13 expression was undetectable in dl-sup6 flowers. These observations suggest that DL and OsMADS13 may function in the same pathway specifying the identity of carpel/ovule and floral meristem. Collectively, we propose a model to illustrate the role of OsMADS3, DL, and OsMADS13 in the specification of flower organ identity and meristem determinacy in rice. Studies in two model eudicot plants, Arabidopsis (Arabidopsis thaliana) and Antirrhinum majus, have suggested that MADS box genes play critical roles in regulating flower development. The proposed genetic ABC model explains how three classes of genes (A, B, and C) work together in specifying floral organ identities (Coen and Meyerowitz, 1991). In Arabidopsis, A (APETALA1 [AP1] and AP2) alone determines sepals, A and B (AP3 and PISTILLATA [PI]) together specify petals, B and C (AGAMOUS [AG]) define stamens, and C alone defines carpels (Coen and Meyerowitz, 1991). Subsequently, two additional classes of genes (D and E) have been included in the modified ABC model.

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“…Тем самым пептид CLV3 способствует дифферен цировке стволовых клеток (Schoof et al, 2000;Katsir et al, 2011;Nimchuk et al, 2011;Yadav et al, 2011). В цветковой меристеме поддержание стволовых клеток носит вре менный характер до момента инициации всех цветковых органов (Prunet et al, 2009). Механизм терминации цвет ковой меристемы включает в себя регуляторную петлю WUS-AGAMOUS (AG) (Lenhard et al, 2001), которая начинается с активации транскрипции AG совместными усилиями WUS и LEAFY (LFY) (Lohmann et al, 2001) и заканчивается репрессией WUS в центре цветковой меристемы одновременно или сразу после инициации плодолистиков (Sun et al, 2009;Liu et al, 2011).…”

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Homeobox genes encoding WOX transcription factors in the flowering parasitic plant Monotropa hypopitys

Щенникова¹,

Shulga²,

Кочиева³

et al. 2017

Vestn. VOGiS

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The formation and maintenance of plant stem cell populations are controlled by the WOX family of homeobox-containing transcription factors. The evolution of WOX genes is considered to be one of the main reasons for flower morphology and plant architecture diversity. The stem cell regulation mechanism is considered to be conserved among flowering plants and most thoroughly studied in Arabidopsis thaliana as a model. The angiosperms morphological diversity implies that there are species-specific features inherent to this mechanism, while the basic signaling is maintained. The unique flowering achlorophyllous mycoheterotrophic plant Monotropa hypopitys obtains nutrients from the tree roots through the mycorrhizal symbiosis. In inductive conditions, the reproductive stem with bracts and an inflorescence at the top is developed from an adventitious root bud. Like other plants, M. hypopitys forms the inflorescence, flower and root meristems, presumably using conserved mechanisms regulating stem cell niche. The study of M. hypopitys homeobox genes should contribute to the knowledge about the function of WOX transcription factors and further understanding of the stem cells control mechanisms in mycoheterotrophic species. The aim of the present study was to analyze M. hypopitys root, bracts and flower transcriptomes obtained from two individual flowering plants. In total, five WOX genes have been identified and characterized by their structure, phylogeny, expression pattern, and possible functions. The assumption is that the MhyWUS1 and MhyWUS2 genes maintain the stem cell population in the inflorescence and flower meristems, MhyWOX13 has a role in the control of root stem cell niche, seed pod formation, flowering initiation, and basic cellular processes, MhyWOX4 functions in the Формирование и поддержание популяций стволовых клеток растения контролируются гомеодомен-содержащими факторами транскрипции семейства WOX. Эволюция гомеобоксных генов, кодирующих данные белки, считается одной из главных причин многообразия форм цветка и морфологии растения в целом. Меха-низм регуляции ниш стволовых клеток в апикальных меристемах признан консервативным для цветковых растений разных видов и наиболее подробно исследован на модели Arabidopsis thaliana. Морфологическое разнообразие покрытосеменных подразумева-ет наличие особенностей этого механизма, присущих отдельным видам, при сохранении основных сигнальных путей. Уникальный представитель покрытосеменных бесхлорофилльный микоге-теротроф подъельник Monotropa hypopitys получает питатель-ные вещества от корней деревьев через микоризный симбиоз. В индук тивных условиях адвентивные репродуктивные почки на корнях M. hypopitys выпускают цветонос с прицветниками и соцве-тием на конце. M. hypopitys так же, как и другие растения, форми-рует меристемы соцветия, цветка и корня, вероятно, используя консервативные пути регуляции ниш стволовых клеток. Изучение гомеобоксных генов такого растения расширит знания о важных эволюционных факторах транскрипции WOX и позволит лучше представлять механизмы...

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Time to Stop: Flower Meristem Termination

Cited by 51 publications

References 89 publications

FAR-RED ELONGATED HYPOCOTYL3 activates SEPALLATA2 but inhibits CLAVATA3 to regulate meristem determinacy and maintenance in Arabidopsis

FAR-RED ELONGATED HYPOCOTYL3 activates SEPALLATA2 but inhibits CLAVATA3 to regulate meristem determinacy and maintenance in Arabidopsis

Genetic Interaction ofOsMADS3,DROOPING LEAF, andOsMADS13in Specifying Rice Floral Organ Identities and Meristem Determinacy

Homeobox genes encoding WOX transcription factors in the flowering parasitic plant Monotropa hypopitys

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