A hierarchical transcriptional network activates specific CDK inhibitors that regulate G2 to control cell size and number in Arabidopsis

Nomoto, Yuji; Takatsuka, Hirotomo; Yamada, Kesuke; Suzuki, Toshiya; Suzuki, Takamasa; Huang, Ying; Latrasse, David; An, Jinpeng; Gombos, Magdolna; Breuer, Christian; Ishida, Takashi; Maeo, Kenichiro; Imamura, Miyu; Yamashino, Takafumi; Sugimoto, Keiko; Magyar, Zoltán; Bögre, László; Raynaud, Cécile; Benhamed, Moussa; Ito, Masaki

doi:10.1038/s41467-022-29316-2

Cited by 31 publications

(68 citation statements)

References 72 publications

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“…The transcript level of SMR9 rose in both comparisons during early olive fruit development, leading to the hypothesis that SMOS1/SMR9 is involved in cell cycle control, quickly triggering the repression of cell division during early olive fruit growth. Recently, [ 83 ] documented that AtSMOS1 forms a dimer with SCARECROW-LIKE28 (SCL28), a GRAS TF that in Arabidopsis, plays a critical part in regulating cell size as part of a transcriptional network downstream of the central MYB3Rs that regulate the G2 to M phase of cell cycle transition. In the present work, the early fruit growth in olive was found to be associated with upregulated SCL28 and MYB3R-1 transcripts ( Figure 6 A).…”

Section: Resultsmentioning

confidence: 99%

Characterization of Transcriptome Dynamics during Early Fruit Development in Olive (Olea europaea L.)

Camarero

Briegas²,

Corbacho³

et al. 2023

IJMS

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In the olive (Olea europaea L.), an economically leading oil crop worldwide, fruit size and yield are determined by the early stages of fruit development. However, few detailed analyses of this stage of fruit development are available. This study offers an extensive characterization of the various processes involved in early olive fruit growth (cell division, cell cycle regulation, and cell expansion). For this, cytological, hormonal, and transcriptional changes characterizing the phases of early fruit development were analyzed in olive fruit of the cv. ‘Picual’. First, the surface area and mitotic activity (by flow cytometry) of fruit cells were investigated during early olive fruit development, from 0 to 42 days post-anthesis (DPA). The results demonstrate that the cell division phase extends up to 21 DPA, during which the maximal proportion of 4C cells in olive fruits was reached at 14 DPA, indicating that intensive cell division was activated in olive fruits at that time. Subsequently, fruit cell expansion lasted as long as 3 weeks more before endocarp lignification. Finally, the molecular mechanisms controlling the early fruit development were investigated by analyzing the transcriptome of olive flowers at anthesis (fruit set) as well as olive fruits at 14 DPA (cell division phase) and at 28 DPA (cell expansion phase). Sequential induction of the cell cycle regulating genes is associated with the upregulation of genes involved in cell wall remodeling and ion fluxes, and with a shift in plant hormone metabolism and signaling genes during early olive fruit development. This occurs together with transcriptional activity of subtilisin-like protease proteins together with transcription factors potentially involved in early fruit growth signaling. This gene expression profile, together with hormonal regulators, offers new insights for understanding the processes that regulate cell division and expansion, and ultimately fruit yield and olive size.

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Section: Resultsmentioning

confidence: 99%

Characterization of Transcriptome Dynamics during Early Fruit Development in Olive (Olea europaea L.)

Camarero

Briegas²,

Corbacho³

et al. 2023

IJMS

View full text Add to dashboard Cite

show abstract

“…For instance, as a key factor in rice tillering, OsMoC1 was involved in the initiation of lateral meristems and the formation and growth of tiller buds [ 30 ]. AtSCL28 has been reported to regulate the balance of cell size and number in Arabidopsis [ 84 ]. The heatmap showed the expression patterns of GRAS genes in different tissues and developmental stages of woodland strawberry, and it was found that at least two-thirds of GRAS genes were highly expressed in various tissues (Fig.…”

Section: Discussionmentioning

confidence: 99%

Evolution and functional analysis of the GRAS family genes in six Rosaceae species

et al. 2022

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Background GRAS genes formed one of the important transcription factor gene families in plants, had been identified in several plant species. The family genes were involved in plant growth, development, and stress resistance. However, the comparative analysis of GRAS genes in Rosaceae species was insufficient. Results In this study, a total of 333 GRAS genes were identified in six Rosaceae species, including 51 in strawberry (Fragaria vesca), 78 in apple (Malus domestica), 41 in black raspberry (Rubus occidentalis), 59 in European pear (Pyrus communis), 56 in Chinese rose (Rosa chinensis), and 48 in peach (Prunus persica). Motif analysis showed the VHIID domain, SAW motif, LR I region, and PFYRE motif were considerably conserved in the six Rosaceae species. All GRAS genes were divided into 10 subgroups according to phylogenetic analysis. A total of 15 species-specific duplicated clades and 3 lineage-specific duplicated clades were identified in six Rosaceae species. Chromosomal localization presented the uneven distribution of GRAS genes in six Rosaceae species. Duplication events contributed to the expression of the GRAS genes, and Ka/Ks analysis suggested the purification selection as a major force during the evolution process in six Rosaceae species. Cis-acting elements and GO analysis revealed that most of the GRAS genes were associated with various environmental stress in six Rosaceae species. Coexpression network analysis showed the mutual regulatory relationship between GRAS and bZIP genes, suggesting the ability of the GRAS gene to regulate abiotic stress in woodland strawberry. The expression pattern elucidated the transcriptional levels of FvGRAS genes in various tissues and the drought and salt stress in woodland strawberry, which were verified by RT-qPCR analysis. Conclusions The evolution and functional analysis of GRAS genes provided insights into the further understanding of GRAS genes on the abiotic stress of Rosaceae species.

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“…While transcript levels of D-type cyclin genes did not differ between ∆ ppshr1∆ppshr2 and wild type, two B-type cyclin genes, whose transcript levels increase during the G2/M phase ( 65 ), exhibited lower transcript levels in Δppshr1Δppshr2. Considering that Arabidopsis SCARECROW-LIKE 28 ( 66 , 67 ), another GRAS family member, regulates cell cycle progression through G2/M and the orientation of cell division, Physcomitrium GRASs may function in the G2/M phase as well.…”

Section: Discussionmentioning

confidence: 99%

GRAS transcription factors regulate cell division planes in moss overriding the default rule

Ishikawa

Fujiwara

Kosetsu

et al. 2023

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

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Plant cells are surrounded by a cell wall and do not migrate, which makes the regulation of cell division orientation crucial for development. Regulatory mechanisms controlling cell division orientation may have contributed to the evolution of body organization in land plants. The GRAS family of transcription factors was transferred horizontally from soil bacteria to an algal common ancestor of land plants. SHORTROOT ( SHR ) and SCARECROW ( SCR ) genes in this family regulate formative periclinal cell divisions in the roots of flowering plants, but their roles in nonflowering plants and their evolution have not been studied in relation to body organization. Here, we show that SHR cell autonomously inhibits formative periclinal cell divisions indispensable for leaf vein formation in the moss Physcomitrium patens , and SHR expression is positively and negatively regulated by SCR and the GRAS member LATERAL SUPPRESSOR , respectively. While precursor cells of a leaf vein lacking SHR usually follow the geometry rule of dividing along the division plane with the minimum surface area, SHR overrides this rule and forces cells to divide nonpericlinally. Together, these results imply that these bacterially derived GRAS transcription factors were involved in the establishment of the genetic regulatory networks modulating cell division orientation in the common ancestor of land plants and were later adapted to function in flowering plant and moss lineages for their specific body organizations.

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A hierarchical transcriptional network activates specific CDK inhibitors that regulate G2 to control cell size and number in Arabidopsis

Cited by 31 publications

References 72 publications

Characterization of Transcriptome Dynamics during Early Fruit Development in Olive (Olea europaea L.)

Characterization of Transcriptome Dynamics during Early Fruit Development in Olive (Olea europaea L.)

Evolution and functional analysis of the GRAS family genes in six Rosaceae species

GRAS transcription factors regulate cell division planes in moss overriding the default rule

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