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The novel function of the Ph1 gene to differentiate homologs from homoeologs evolved in Triticum turgidum ssp. dicoccoides via a dramatic meiosis-specific increase in the expression of the 5B copy of the C-Ph1 gene

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Abstract

The Ph1 gene is the principal regulator of homoeologous chromosome pairing control (HECP) that ensures the diploid-like meiotic chromosome pairing behavior of polyploid wheat. The HECP control was speculated to have evolved after the first event of polyploidization. With the objective to accurately understand the evolution of the HECP control, wild emmer wheat accessions previously known to differ for HECP control were characterized for the structure and expression of the candidate Ph1 gene, C-Ph1. The C-TdPh1-5A and 5B gene copies of emmer wheat showed 98 and 99% DNA sequence similarity respectively with the corresponding hexaploid wheat copies. Further, the C-TdPh1-5B carried the C-Ph1-5B specific structural changes and transcribed three splice variants as observed in the hexaploid wheat. Further, single nucleotide changes differentiating accessions varying for HECP control were identified. Analyzed by quantitative expression analysis, the wild emmer accessions with HECP control showed ~ 10,000-fold higher transcript abundance of the C-TdPh1-5B copy during prophase-I compared to accessions lacking the control. Differential transcriptional regulation of C-TdPh1-5B splice variants further revealed that C-Ph1-5Balt1 variant is mainly responsible for differential accumulation of C-Ph1-5B copy in accessions with HECP control. Taken together, these results showed that the HECP control evolved via transcriptional regulation of splice variants during meiosis.

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Acknowledgments

We would like to thank Dr. Moshe Feldman for kindly sharing the germplasm.

Author’s contribution

KS and KSG designed the research. KS and MAK performed the experiments and data analysis. KS and KSG wrote the manuscript. KS, MAK, and KSG critically revised the manuscript.

Funding

This work was supported by USDA National Institute of Food and Agriculture (Hatch project number WNP00449) and United States Agency for International Development Feed the Future Innovation Lab-Climate Resilient Wheat (Grant number AID-OAA-A-13-00008).

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Authors and Affiliations

  1. Department of Crop and Soil Sciences, Washington State University, Pullman, WA, USA

    Kanwardeep S. Rawale, Muhammad A. Khan & Kulvinder S. Gill

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  1. Kanwardeep S. Rawale
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  2. Muhammad A. Khan
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  3. Kulvinder S. Gill
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Correspondence to Kulvinder S. Gill.

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Summary:

Ph1 locus plays a very critical role in chromosome pairing and recombination in polyploid wheat. The Ph1 locus prohibits recombination between chromosomes of polyploid wheat and its wild relatives leading to restricted or no crossing over. Thus, making it difficult to transfer gene(s) of interest from wild relatives to cultivated wheat. Until recently, very limited information is available about the gene controlling the phenotype. Recent identification of candidate Ph1 (C-Ph1) paved the way for further understanding its evolution, and mechanism of action would pave the way for its targeted use in wheat crop improvement. In this study, we have identified the major transcript regulating C-Ph1 gene expression that can be used in future studies for targeted manipulation of recombination to transfer biotic and abiotic stress tolerance from wild relatives of polyploid wheat.

Electronic supplementary material

Fig. S1

Multiple sequence alignment of C-TdPh1 and C-TaPh1 gene homoeologs around major copy specific structural changes (29 bp deletion and 60 bp insertion) highlighting conservation of gene structure in hexaploid and tetraploid wheat. (PNG 292 kb)

High resolution image (TIF 1673 kb)

Fig. S2

Multiple sequence alignment of C-TdPh1-5B gene sequence from wild emmer wheat accessions varying for homoeologous chromosome pairing control for the region carrying 29 bp deletion and 60 bp insertion. (PNG 48 kb)

High resolution image (TIF 1856 kb)

Fig. S3

Multiple sequence alignment of C-Ph1-5A copy from wild emmer wheat accessions varying for HECP control. Sequence conservation at a site is highlighted with asterisk (*) at the bottom, whereas sequence change between wild emmer wheat and hexaploid wheat is highlighted with black rectangular box and asterisk (*) on top of the box. Single nucleotide variants differentiating –HECP and + HECP lines are highlighted with blue rectangular boxes and asterisk (*) on the top of the box. (PNG 275 kb)

High resolution image (TIF 2.09 mb)

Fig. S4

Multiple sequence alignment of C-Ph1-5B copy from wild emmer wheat accessions varying for HECP control. Sequence conservation at a site is highlighted with asterisk (*) at the bottom, whereas sequence change between wild emmer wheat and hexaploid wheat is highlighted with black rectangular box and asterisk (*) on top of the box. Single nucleotide variants differentiating –HECP and + HECP lines are highlighted with blue rectangular boxes and asterisk (*) on the top of the box. (PNG 357 kb)

High resolution image (TIF 5724 kb)

Supplementary Table 1

(DOCX 13 kb)

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Rawale, K.S., Khan, M.A. & Gill, K.S. The novel function of the Ph1 gene to differentiate homologs from homoeologs evolved in Triticum turgidum ssp. dicoccoides via a dramatic meiosis-specific increase in the expression of the 5B copy of the C-Ph1 gene. Chromosoma 128, 561–570 (2019). https://doi.org/10.1007/s00412-019-00724-6

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