Modeling the Flowering Activation Motif during Vernalization in Legumes: A Case Study of <i>M. trancatula</i>

In many plant species, flowering is promoted by the cold treatment or vernalization. The mechanism of vernalization-induced flowering has been extensively studied in <i>Arabidopsis</i> but remains largely unknown in legumes. The orthologs of the <i>FLC</i> gene, a major regul...

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Main Authors: Maria A. Duk, Vitaly V. Gursky, Maria G. Samsonova, Svetlana Yu. Surkova
Format: Article
Language:English
Published: MDPI AG 2023-12-01
Series:Life
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Online Access:https://www.mdpi.com/2075-1729/14/1/26
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author Maria A. Duk
Vitaly V. Gursky
Maria G. Samsonova
Svetlana Yu. Surkova
author_facet Maria A. Duk
Vitaly V. Gursky
Maria G. Samsonova
Svetlana Yu. Surkova
author_sort Maria A. Duk
collection DOAJ
description In many plant species, flowering is promoted by the cold treatment or vernalization. The mechanism of vernalization-induced flowering has been extensively studied in <i>Arabidopsis</i> but remains largely unknown in legumes. The orthologs of the <i>FLC</i> gene, a major regulator of vernalization response in <i>Arabidopsis</i>, are absent or non-functional in the vernalization-sensitive legume species. Nevertheless, the legume integrator genes <i>FT</i> and <i>SOC1</i> are involved in the transition of the vernalization signal to meristem identity genes, including <i>PIM</i> (<i>AP1</i> ortholog). However, the regulatory contribution of these genes to <i>PIM</i> activation in legumes remains elusive. Here, we presented the theoretical and data-driven analyses of a feed-forward regulatory motif that includes a vernalization-responsive <i>FT</i> gene and several <i>SOC1</i> genes, which independently activate <i>PIM</i> and thereby mediate floral transition. Our theoretical model showed that the multiple regulatory branches in this regulatory motif facilitated the elimination of no-sense signals and amplified useful signals from the upstream regulator. We further developed and analyzed four data-driven models of <i>PIM</i> activation in <i>Medicago trancatula</i> in vernalized and non-vernalized conditions in wild-type and <i>fta1-1</i> mutants. The model with <i>FTa1</i> providing both direct activation and indirect activation via three intermediate activators, <i>SOC1a</i>, <i>SOC1b</i>, and <i>SOC1c</i>, resulted in the most relevant <i>PIM</i> dynamics. In this model, the difference between regulatory inputs of <i>SOC1</i> genes was nonessential. As a result, in the <i>M. trancatula</i> model, the cumulative action of <i>SOC1a</i>, <i>SOC1b</i>, and <i>SOC1c</i> was favored. Overall, in this study, we first presented the in silico analysis of vernalization-induced flowering in legumes. The considered vernalization network motif can be supplemented with additional regulatory branches as new experimental data become available.
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spelling doaj.art-29f0baf6de5a4636b9ac24c97f5b52262024-01-26T17:20:27ZengMDPI AGLife2075-17292023-12-011412610.3390/life14010026Modeling the Flowering Activation Motif during Vernalization in Legumes: A Case Study of <i>M. trancatula</i>Maria A. Duk0Vitaly V. Gursky1Maria G. Samsonova2Svetlana Yu. Surkova3Mathematical Biology and Bioinformatics Laboratory, Peter the Great Saint Petersburg Polytechnic University, 195251 St. Petersburg, RussiaTheoretical Department, Ioffe Institute, 194021 St. Petersburg, RussiaMathematical Biology and Bioinformatics Laboratory, Peter the Great Saint Petersburg Polytechnic University, 195251 St. Petersburg, RussiaMathematical Biology and Bioinformatics Laboratory, Peter the Great Saint Petersburg Polytechnic University, 195251 St. Petersburg, RussiaIn many plant species, flowering is promoted by the cold treatment or vernalization. The mechanism of vernalization-induced flowering has been extensively studied in <i>Arabidopsis</i> but remains largely unknown in legumes. The orthologs of the <i>FLC</i> gene, a major regulator of vernalization response in <i>Arabidopsis</i>, are absent or non-functional in the vernalization-sensitive legume species. Nevertheless, the legume integrator genes <i>FT</i> and <i>SOC1</i> are involved in the transition of the vernalization signal to meristem identity genes, including <i>PIM</i> (<i>AP1</i> ortholog). However, the regulatory contribution of these genes to <i>PIM</i> activation in legumes remains elusive. Here, we presented the theoretical and data-driven analyses of a feed-forward regulatory motif that includes a vernalization-responsive <i>FT</i> gene and several <i>SOC1</i> genes, which independently activate <i>PIM</i> and thereby mediate floral transition. Our theoretical model showed that the multiple regulatory branches in this regulatory motif facilitated the elimination of no-sense signals and amplified useful signals from the upstream regulator. We further developed and analyzed four data-driven models of <i>PIM</i> activation in <i>Medicago trancatula</i> in vernalized and non-vernalized conditions in wild-type and <i>fta1-1</i> mutants. The model with <i>FTa1</i> providing both direct activation and indirect activation via three intermediate activators, <i>SOC1a</i>, <i>SOC1b</i>, and <i>SOC1c</i>, resulted in the most relevant <i>PIM</i> dynamics. In this model, the difference between regulatory inputs of <i>SOC1</i> genes was nonessential. As a result, in the <i>M. trancatula</i> model, the cumulative action of <i>SOC1a</i>, <i>SOC1b</i>, and <i>SOC1c</i> was favored. Overall, in this study, we first presented the in silico analysis of vernalization-induced flowering in legumes. The considered vernalization network motif can be supplemented with additional regulatory branches as new experimental data become available.https://www.mdpi.com/2075-1729/14/1/26vernalizationlegumesgene networksdynamical modelfeed-forward loop<i>Medicago trancatula</i>
spellingShingle Maria A. Duk
Vitaly V. Gursky
Maria G. Samsonova
Svetlana Yu. Surkova
Modeling the Flowering Activation Motif during Vernalization in Legumes: A Case Study of <i>M. trancatula</i>
Life
vernalization
legumes
gene networks
dynamical model
feed-forward loop
<i>Medicago trancatula</i>
title Modeling the Flowering Activation Motif during Vernalization in Legumes: A Case Study of <i>M. trancatula</i>
title_full Modeling the Flowering Activation Motif during Vernalization in Legumes: A Case Study of <i>M. trancatula</i>
title_fullStr Modeling the Flowering Activation Motif during Vernalization in Legumes: A Case Study of <i>M. trancatula</i>
title_full_unstemmed Modeling the Flowering Activation Motif during Vernalization in Legumes: A Case Study of <i>M. trancatula</i>
title_short Modeling the Flowering Activation Motif during Vernalization in Legumes: A Case Study of <i>M. trancatula</i>
title_sort modeling the flowering activation motif during vernalization in legumes a case study of i m trancatula i
topic vernalization
legumes
gene networks
dynamical model
feed-forward loop
<i>Medicago trancatula</i>
url https://www.mdpi.com/2075-1729/14/1/26
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