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The intervening domain is required for DNA-binding and functional identity of plant MADS transcription factors.

ABSTRACT: The MADS transcription factors (TF) are an ancient eukaryotic protein family. In plants, the family is divided into two main lineages. Here, we demonstrate that DNA binding in both lineages absolutely requires a short amino acid sequence C-terminal to the MADS domain (M domain) called the Intervening domain (I domain) that was previously defined only in type II lineage MADS. Structural elucidation of the MI domains from the floral regulator, SEPALLATA3 (SEP3), shows a conserved fold with the I domain acting to stabilise the M domain. Using the floral organ identity MADS TFs, SEP3, APETALA1 (AP1) and AGAMOUS (AG), domain swapping demonstrate that the I domain alters genome-wide DNA-binding specificity and dimerisation specificity. Introducing AG carrying the I domain of AP1 in the Arabidopsis ap1 mutant resulted in strong complementation and restoration of first and second whorl organs. Taken together, these data demonstrate that the I domain acts as an integral part of the DNA-binding domain and significantly contributes to the functional identity of the MADS TF.

SUBMITTER: Lai X

PROVIDER: S-EPMC8346517 | biostudies-literature | 2021 Aug

REPOSITORIES: biostudies-literature

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The intervening domain is required for DNA-binding and functional identity of plant MADS transcription factors.

Lai Xuelei X Vega-Léon Rosario R Hugouvieux Veronique V Blanc-Mathieu Romain R van der Wal Froukje F Lucas Jérémy J Silva Catarina S CS Jourdain Agnès A Muino Jose M JM Nanao Max H MH Immink Richard R Kaufmann Kerstin K Parcy François F Smaczniak Cezary C Zubieta Chloe C

Nature communications 20210806 1

The MADS transcription factors (TF) are an ancient eukaryotic protein family. In plants, the family is divided into two main lineages. Here, we demonstrate that DNA binding in both lineages absolutely requires a short amino acid sequence C-terminal to the MADS domain (M domain) called the Intervening domain (I domain) that was previously defined only in type II lineage MADS. Structural elucidation of the MI domains from the floral regulator, SEPALLATA3 (SEP3), shows a conserved fold with the I d ...[more]

PMID: 34362909

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Project description:Plants MADS-domain/AGL proteins constitute a large transcription factor (TF) family that controls the development of almost every plant organ. We performed a phylogeny of (ca. 500) MADS-domain proteins from Arabidopsis and four legume species. We identified clades with Arabidopsis MADS-domain proteins known to participate in root development that grouped legume MADS-proteins with similar high expression in roots and nodules. In this work, we analyzed the role of AGL transcription factors in the common bean (Phaseolus vulgaris) - Rhizobium etli N-fixing symbiosis. Sixteen P. vulgaris AGL genes (PvAGL), out of 93 family members, are expressed - at different levels - in roots and nodules. From there, we selected the PvAGL gene denominated PvFUL-like for overexpression or silencing in composite plants, with transgenic roots and nodules, that were used for phenotypic analysis upon inoculation with Rhizobium etli. Because of sequence identity in the DNA sequence used for RNAi-FUL-like construct, roots, and nodules expressing this construct -referred to as RNAi_AGL- showed lower expression of other five PvAGL genes highly expressed in roots/nodules. Contrasting with PvFUL-like overexpressing plants, rhizobia-inoculated plants expressing the RNAi_AGL silencing construct presented affection in the generation and growth of transgenic roots from composite plants, both under non-inoculated or rhizobia-inoculated condition. Furthermore, the rhizobia-inoculated plants showed decreased rhizobial infection concomitant with the lower expression level of early symbiotic genes and increased number of small, ineffective nodules that indicate an alteration in the autoregulation of the nodulation symbiotic process. We propose that the positive effects of PvAGL TF in the rhizobia symbiotic processes result from its potential interplay with NIN, the master symbiotic TF regulator, that showed a CArG-box consensus DNA sequence recognized for DNA binding of AGL TF and presented an increased or decreased expression level in roots from non-inoculated plants transformed with OE_FUL or RNAi_AGL construct, respectively. Our work contributes to defining novel transcriptional regulators for the common bean - rhizobia N-fixing symbiosis, a relevant process for sustainable agriculture.

Dataset Information

The intervening domain is required for DNA-binding and functional identity of plant MADS transcription factors.

Publications

The intervening domain is required for DNA-binding and functional identity of plant MADS transcription factors.

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