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. 2020 Mar;133(3):809-828.
doi: 10.1007/s00122-019-03508-9. Epub 2019 Dec 18.

Dmc1 Is a Candidate for Temperature Tolerance During Wheat Meiosis

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Free PMC article

Dmc1 Is a Candidate for Temperature Tolerance During Wheat Meiosis

Tracie Draeger et al. Theor Appl Genet. .
Free PMC article

Abstract

The meiotic recombination gene Dmc1 on wheat chromosome 5D has been identified as a candidate for the maintenance of normal chromosome synapsis and crossover at low and possibly high temperatures. We initially assessed the effects of low temperature on meiotic chromosome synapsis and crossover formation in the hexaploid wheat (Triticum aestivum L.) variety 'Chinese Spring'. At low temperatures, asynapsis and chromosome univalence have been observed before in Chinese Spring lines lacking the long arm of chromosome 5D (5DL), which led to the proposal that 5DL carries a gene (Ltp1) that stabilises wheat chromosome pairing at low temperatures. In the current study, Chinese Spring wild type and 5DL interstitial deletion mutant plants were exposed to low temperature in a controlled environment room during a period from premeiotic interphase to early meiosis I. A 5DL deletion mutant was identified whose meiotic chromosomes exhibit extremely high levels of asynapsis and chromosome univalence at metaphase I after 7 days at 13 °C, suggesting that Ltp1 is deleted in this mutant. Immunolocalisation of the meiotic proteins ASY1 and ZYP1 on ltp1 mutants showed that low temperature results in a failure to complete synapsis at pachytene. KASP genotyping revealed that the ltp1 mutant has a 4-Mb deletion in 5DL. Of 41 genes within this deletion region, the strongest candidate for the stabilisation of chromosome pairing at low temperatures is the meiotic recombination gene Dmc1. The ltp1 mutants were subsequently treated at 30 °C for 24 h during meiosis and exhibited a reduced number of crossovers and increased univalence, though to a lesser extent than at 13 °C. We therefore renamed our ltp1 mutant 'ttmei1' (temperature-tolerant meiosis 1) to reflect this additional loss of high temperature tolerance.

Conflict of interest statement

The authors declare that they have no conflict of interest.

Figures

Fig. 1
Fig. 1
Map of wheat chromosome arm 5DL showing locations of deletions detected using 5DL-specific KASP markers (black or red text with BA prefix) or microsatellite markers (blue); markers are aligned with positions on the Chinese Spring IWGSC RefSeq v1.0 genome assembly (shown in Mb); yellow boxes mark the extent of the 5DL terminal deletions in lines with normal pairing at 13 °C; breakpoints of terminal deletion lines are indicated by blue arrows; pink boxes show positions of 5DL interstitial deletions in lines with normal pairing at 13 °C; orange boxes show the location of the 5DL deletion in the mutant line 22-F5 (ttmei1), which exhibits asynapsis at 13 °C; small grey box shows the ttmei1 deletion region and its flanking markers (in red) as detected in the initial KASP genotyping analysis with the only marker deleted in ttmei1 (BA00822801) shown in bold text; larger grey inset box shows fine mapping between flanking markers BA00334971 and BA00808441 (red text) using BA00822801 and 25 additional KASP markers. Markers shown in orange boxes are deleted in the ttmei1 mutant. The position of the candidate gene TaDmc1-D1 (green box) at 225 Mb is indicated with a black arrow
Fig. 2
Fig. 2
Feulgen-stained metaphase I chromosomes from PMCs of wild-type Chinese Spring, 22-F5 (ttmei1) mutant and N5DT5B plants treated at different temperatures. a wild type, bttmei1 and c N5DT5B at normal temperatures; d wild type, ettmei1 and f N5DT5B after 7 days at 13 °C; g wild type and h and ittmei1 after 24 h at 30 °C. Examples of univalent chromosomes (univ), rod bivalents (rod), ring bivalents (ring), multivalents (multiv), single chiasma (X), double chiasmata (XX) and sticky, clumping chromosomes (clump) are indicated with arrows; note complete univalence in ttmei1 and N5DT5B after treatment at 13 °C. Scale bars, 10 μm
Fig. 3
Fig. 3
Bar charts showing genotypic effects on meiotic metaphase I chromosomes of Chinese Spring (CS) wild-type and 22-F5 (ttmei1) mutant plants after treatment at 20 °C, 13 °C and 30 °C. The numbers of univalents, ring and rod bivalents and single crossovers are shown. Multivalents and double crossovers are not shown
Fig. 4
Fig. 4
Bar charts showing the effects of three different temperature treatments (20 °C, 13 °C and 30 °C) on meiotic metaphase I chromosomes of Chinese Spring (CS) wild-type and 22-F5 (ttmei1) mutant plants. The numbers of univalents, ring and rod bivalents and single crossovers are shown. Multivalents and double crossovers are not shown
Fig. 5
Fig. 5
Immunolocalisation of meiotic proteins ASY1 (green) and ZYP1 (magenta) in PMCs from wheat Chinese Spring wild type (a) and ttmei1 mutant (b), both under low-temperature conditions. a During early zygotene, synapsis starts from the telomeres at one pole of the nucleus in wild-type wheat. During pachytene, all chromosomes have synapsed. ASY1 labelling in green shows that a very small proportion of chromatin has not yet synapsed. b In ttmei1 mutants, synapsis initiates normally at one pole of the nucleus; however, synapsis is soon compromised and is not completed. Therefore, there is no normal pachytene in the ttmei1 mutant. DAPI staining in blue. Scale bar, 10 μm
Fig. 6
Fig. 6
TaDmc1 gene structure and amino-acid sequence alignment. a Exon–intron structure of the three TaDmc1 homeologs. b Multiple sequence alignment of amino acids from DMC1 proteins of different cereal plants: hexaploid wheat (Triticum aestivum cv Chinese Spring; Ta), barley (Hordeum vulgare; Hv) and rice (Oryza sativa Japonica; Os). SNPs are shown in red text on a grey background. Symbols below each position in the sequence indicate the amount of conservation (asterisk ‘*’: identical residues; colon ‘:’: conserved substitution; period ‘.’: semi-conserved substitution; and space ‘ ’: not conserved). A single amino-acid substitution in TaDMC1-D1 at position 114 (indicated by a large red triangle) may confer low temperature tolerance in wheat. Small blue triangles show the positions of three other amino-acid substitutions in TaDMC1-B1 at positions 167, 214 and 316, and a small green triangle shows the position of a substitution in TaDMC1-A1 at position 310

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