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Neo-functionalization of a Teosinte branched 1 homologue mediates adaptations of upland rice.

ABSTRACT: The rice orthologue of maize domestication gene Teosinte branched 1 (Tb1) affects tillering. But, unlike maize Tb1 gene, it was not selected during domestication. Here, we report that an OsTb1 duplicate gene (OsTb2) has been artificially selected during upland rice adaptation and that natural variation in OsTb2 is associated with tiller number. Interestingly, transgenic rice overexpressing this gene shows increased rather than decreased tillering, suggesting that OsTb2 gains a regulatory effect opposite to that of OsTb1 following duplication. Functional analyses suggest that the OsTb2 protein positively regulates tillering by interacting with the homologous OsTb1 protein and counteracts the inhibitory effect of OsTb1 on tillering. We further characterize two functional variations within OsTb2 that regulate protein function and gene expression, respectively. These results not only present an example of neo-functionalization that generates an opposite function following duplication but also suggest that the Tb1 homologue has been selected in upland rice.

SUBMITTER: Lyu J

PROVIDER: S-EPMC7002408 | biostudies-literature | 2020 Feb

REPOSITORIES: biostudies-literature

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Neo-functionalization of a Teosinte branched 1 homologue mediates adaptations of upland rice.

Lyu Jun J Huang Liyu L Zhang Shilai S Zhang Yesheng Y He Weiming W Zeng Peng P Zeng Yan Y Huang Guangfu G Zhang Jing J Ning Min M Bao Yachong Y Zhao Shilei S Fu Qi Q Wade Len J LJ Chen Hua H Wang Wen W Hu Fengyi F

Nature communications 20200205 1

The rice orthologue of maize domestication gene Teosinte branched 1 (Tb1) affects tillering. But, unlike maize Tb1 gene, it was not selected during domestication. Here, we report that an OsTb1 duplicate gene (OsTb2) has been artificially selected during upland rice adaptation and that natural variation in OsTb2 is associated with tiller number. Interestingly, transgenic rice overexpressing this gene shows increased rather than decreased tillering, suggesting that OsTb2 gains a regulatory effect ...[more]

PMID: 32024833

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Project description:BackgroundStrigolactones (SLs) are a class of plant hormones that control many aspects of plant growth. The SL signalling mechanism is homologous to that of karrikins (KARs), smoke-derived compounds that stimulate seed germination. In angiosperms, the SL receptor is an α/β-hydrolase known as DWARF14 (D14); its close homologue, KARRIKIN INSENSITIVE2 (KAI2), functions as a KAR receptor and likely recognizes an uncharacterized, endogenous signal ('KL'). Previous phylogenetic analyses have suggested that the KAI2 lineage is ancestral in land plants, and that canonical D14-type SL receptors only arose in seed plants; this is paradoxical, however, as non-vascular plants synthesize and respond to SLs.ResultsWe have used a combination of phylogenetic and structural approaches to re-assess the evolution of the D14/KAI2 family in land plants. We analysed 339 members of the D14/KAI2 family from land plants and charophyte algae. Our phylogenetic analyses show that the divergence between the eu-KAI2 lineage and the DDK (D14/DLK2/KAI2) lineage that includes D14 occurred very early in land plant evolution. We show that eu-KAI2 proteins are highly conserved, and have unique features not found in DDK proteins. Conversely, we show that DDK proteins show considerable sequence and structural variation to each other, and lack clearly definable characteristics. We use homology modelling to show that the earliest members of the DDK lineage structurally resemble KAI2 and that SL receptors in non-seed plants likely do not have D14-like structure. We also show that certain groups of DDK proteins lack the otherwise conserved MORE AXILLARY GROWTH2 (MAX2) interface, and may thus function independently of MAX2, which we show is highly conserved throughout land plant evolution.ConclusionsOur results suggest that D14-like structure is not required for SL perception, and that SL perception has relatively relaxed structural requirements compared to KAI2-mediated signalling. We suggest that SL perception gradually evolved by neo-functionalization within the DDK lineage, and that the transition from KAI2-like to D14-like protein may have been driven by interactions with protein partners, rather than being required for SL perception per se.

Project description:Adaptation of crops to climate change has motivated an increasing interest in the potential value of novel traits from wild species; maize wild relatives, the teosintes, harbor traits that may be useful to maize breeding. To study the ecogeographic distribution of teosinte we constructed a robust database of 2363 teosinte occurrences from published sources for the period 1842-2016. A geographical information system integrating 216 environmental variables was created for Mexico and Central America and was used to characterize the environment of each teosinte occurrence site. The natural geographic distribution of teosinte extends from the Western Sierra Madre of the State of Chihuahua, Mexico to the Pacific coast of Nicaragua and Costa Rica, including practically the entire western part of Mesoamerica. The Mexican annuals Zea mays ssp. parviglumis and Zea mays ssp. mexicana show a wide distribution in Mexico, while Zea diploperennis, Zea luxurians, Zea perennis, Zea mays ssp. huehuetenangensis, Zea vespertilio and Zea nicaraguensis had more restricted and distinct ranges, representing less than 20% of the total occurrences. Only 11.2% of teosinte populations are found in Protected Natural Areas in Mexico and Central America. Ecogeographical analysis showed that teosinte can cope with extreme levels of precipitation and temperatures during growing season. Modelling teosinte geographic distribution demonstrated congruence between actual and potential distributions; however, some areas with no occurrences appear to be within the range of adaptation of teosintes. Field surveys should be prioritized to such regions to accelerate the discovery of unknown populations. Potential areas for teosintes Zea mays ssp. mexicana races Chalco, Nobogame, and Durango, Zea mays ssp. huehuetenangensis, Zea luxurians, Zea diploperennis and Zea nicaraguensis are geographically separated; however, partial overlapping occurs between Zea mays ssp. parviglumis and Zea perennis, between Zea mays ssp. parviglumis and Zea diploperennis, and between Zea mays ssp. mexicana race Chalco and Zea mays ssp. mexicana race Central Plateau. Assessing priority of collecting for conservation showed that permanent monitoring programs and in-situ conservation projects with participation of local farmer communities are critically needed; Zea mays ssp. mexicana (races Durango and Nobogame), Zea luxurians, Zea diploperennis, Zea perennis and Zea vespertilio should be considered as the highest priority taxa.

Dataset Information

Neo-functionalization of a Teosinte branched 1 homologue mediates adaptations of upland rice.

Publications

Neo-functionalization of a Teosinte branched 1 homologue mediates adaptations of upland rice.

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