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Coactivation of antagonistic genes stabilizes polarity patterning during shoot organogenesis.

ABSTRACT: Spatiotemporal patterns of gene expression are instrumental to morphogenesis. A stable pattern interface, often between reciprocal-inhibiting morphogens, must be robustly maintained after initial patterning cues diminish, organ growth, or organ geometry changes. In plants, floral and leaf primordia obtain the adaxial-abaxial pattern at the shoot apical meristem periphery. However, it is unknown how the pattern is maintained after primordia have left the shoot apex. Here, through a combination of computational simulations, time-lapse imaging, and genetic analysis, we propose a model in which auxin simultaneously promotes both adaxial and abaxial domains of expression. Furthermore, we identified multilevel feedback regulation of auxin signaling to refine the spatiotemporal patterns. Our results demonstrate that coactivation by auxin determines and stabilizes antagonistic adaxial-abaxial patterning during aerial organ formation.

SUBMITTER: Guan C

PROVIDER: S-EPMC9176745 | biostudies-literature | 2022 Jun

REPOSITORIES: biostudies-literature

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Coactivation of antagonistic genes stabilizes polarity patterning during shoot organogenesis.

Guan Chunmei C Qiao Lingxia L Xiong Yuanyuan Y Zhang Lei L Jiao Yuling Y

Science advances 20220608 23

Spatiotemporal patterns of gene expression are instrumental to morphogenesis. A stable pattern interface, often between reciprocal-inhibiting morphogens, must be robustly maintained after initial patterning cues diminish, organ growth, or organ geometry changes. In plants, floral and leaf primordia obtain the adaxial-abaxial pattern at the shoot apical meristem periphery. However, it is unknown how the pattern is maintained after primordia have left the shoot apex. Here, through a combination of ...[more]

PMID: 35675392

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Project description:BackgroundOur aim is to improve knowledge of gene regulatory circuits important to dedifferentiation, redifferentiation, and adventitious meristem organization during in vitro regeneration of plants. Regeneration of transgenic cells remains a major obstacle to research and commercial deployment of most taxa of transgenic plants, and woody species are particularly recalcitrant. The model woody species Populus, due to its genome sequence and amenability to in vitro manipulation, is an excellent species for study in this area. The genes recognized may help to guide the development of new tools for improving the efficiency of plant regeneration and transformation.ResultsWe analyzed gene expression during poplar in vitro dedifferentiation and shoot regeneration using an Affymetrix array representing over 56,000 poplar transcripts. We focused on callus induction and shoot formation, thus we sampled RNAs from tissues: prior to callus induction, 3 days and 15 days after callus induction, and 3 days and 8 days after the start of shoot induction. We used a female hybrid white poplar clone (INRA 717-1 B4, Populus tremula x P. alba) that is used widely as a model transgenic genotype. Approximately 15% of the monitored genes were significantly up-or down-regulated when controlling the false discovery rate (FDR) at 0.01; over 3,000 genes had a 5-fold or greater change in expression. We found a large initial change in expression after the beginning of hormone treatment (at the earliest stage of callus induction), and then a much smaller number of additional differentially expressed genes at subsequent regeneration stages. A total of 588 transcription factors that were distributed in 45 gene families were differentially regulated. Genes that showed strong differential expression included components of auxin and cytokinin signaling, selected cell division genes, and genes related to plastid development and photosynthesis. When compared with data on in vitro callogenesis in Arabidopsis, 25% (1,260) of up-regulated and 22% (748) of down-regulated genes were in common with the genes regulated in poplar during callus induction.ConclusionThe major regulatory events during plant cell organogenesis occur at early stages of dedifferentiation. The regulatory circuits reflect the combinational effects of transcriptional control and hormone signaling, and associated changes in light environment imposed during dedifferentiation.

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Coactivation of antagonistic genes stabilizes polarity patterning during shoot organogenesis.

Publications

Coactivation of antagonistic genes stabilizes polarity patterning during shoot organogenesis.

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