Natural selection of a GSK3 determines rice mesocotyl domestication by coordinating strigolactone and brassinosteroid signaling

Shiyong Sun,Xiaoming Li,Linlin Wang,Xuelu Wang,Yancui Jia,Tao Wang,Weibo Xie,Chang Liu,Xuehui Huang

doi:10.1038/s41467-018-04952-9

Shiyong Sun, Xiaoming Li + Show 7 more

Open Access

https://doi.org/10.1038/s41467-018-04952-9

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Abstract

Mesocotyl is the crucial organ for pushing buds out of deep water or soil after germination in monocots. Deep direct seeding or mechanized dry seeding cultivation practice requires rice cultivars having long mesocotyl. However, the mechanisms of mesocotyl elongation and domestication remain unknown. Here, our genome-wide association study (GWAS) reveals that natural variations of OsGSK2, a conserved GSK3-like kinase involved in brassinosteroid signaling, determine rice mesocotyl length variation. Variations in the coding region of OsGSK2 alter its kinase activity. It is selected for mesocotyl length variation during domestication. Molecular analyses show that brassinosteroid-promoted mesocotyl elongation functions by suppressing the phosphorylation of an U-type cyclin, CYC U2, by OsGSK2. Importantly, the F-box protein D3, a major positive component in strigolactone signaling, can degrade the OsGSK2-phosphorylated CYC U2 to inhibit mesocotyl elongation. Together, these results suggest that OsGSK2 is selected to regulate mesocotyl length by coordinating strigolactone and brassinosteroid signaling during domestication.

Highlights

Mesocotyl is the crucial organ for pushing buds out of deep water or soil after germination in monocots
To identify single-nucleotide polymorphism (SNP) in OsGSK2 associated with the natural variation in mesocotyl length, we first analyzed the SNPs in the OsGSK2 promoter regions (2.0 kb region upstream of the translation start site) from 504 rice accessions
The different phosphorylation levels in BZR1/ BES1 can be distinguished by different protein sizes using western blot[22,23], which has been widely used to evaluate the kinase activity of OsGSK2/BIN2

Summary

Introduction

Mesocotyl is the crucial organ for pushing buds out of deep water or soil after germination in monocots. The F-box protein D3, a major positive component in strigolactone signaling, can degrade the OsGSK2-phosphorylated CYC U2 to inhibit mesocotyl elongation. Together, these results suggest that OsGSK2 is selected to regulate mesocotyl length by coordinating strigolactone and brassinosteroid signaling during domestication. We perform a genome-wide association study (GWAS) for rice mesocotyl length and demonstrate that natural alleles of OsGSK2 in coding regions with the different kinase activities address mesocotyl variation and domestication from Oryza rufipogon to the cultivated rice; BRs promote mesocotyl elongation via cell division controlled by CYC U2, a plant-specific U-type cyclin, and OsGSK2 can phosphorylate CYC U2 to reduce its protein stability. Our findings reveal an important mechanism in mesocotyl elongation coordinately controlled by SL and BR signaling, and indicate that OsGSK2 is a key locus under the selection for mesocotyl length variation during rice domestication

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