Phylogeographic and quantitative trait locus analysis of the ability of Aegilops tauschii Coss., the D genome progenitor of common wheat, to cause genome doubling in the F1 hybrids with Triticum turgidum L., the AB genome progenitor

327

Bartoń K (2019) MuMIn: Multi-Model Inference. R package version 1.43.6.

328

https://CRAN.R-project.org/package=MuMIn. Accessed 16 March 2020

329

330

Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using

331

lme4.

332

https://www.jstatsoft.org/article/view/v067i01

Journal

of

Statistical

10

Software

67:1–48.

333

334

Broman KW, Wu H, Sen Ś, Churchill GA (2003) R/qtl: QTL mapping in experimental

335

crosses.

336

https://academic.oup.com/bioinformatics/article/19/7/889/197785

Bioinformatics

19:889–890.

337

338

Devisetty UK, Mayes K, Mayes S. (2010) The RAD51 and DMC1 homoeologous genes

339

of bread wheat: cloning, molecular characterization and expression analysis. BMC

340

Research Notes 3:245. https://bmcresnotes.biomedcentral.com/articles/10.1186/1756-

341

0500-3-245

342

343

Gaurav K, Arora S, Silva P, Sanchez-Martin J, Horsnell R, Gao L, Brar GS, Widrig V,

344

Raupp J, Singh N, et al. (2021) Evolution of the bread wheat D-subgenome and enriching

345

it

346

https://www.biorxiv.org/content/10.1101/2021.01.31.428788v2

with

diversity

from

Aegilops

tauschii.

bioRxiv.

347

348

Gogniashvili M, Jinjikhadze T, Maisaia I, Akhalkatsi M, Kotorashvili A, Kotaria N, Beridze

349

T, Dudnikov A. Ju. (2016) Complete chloroplast genomes of Aegilops tauschii Coss. and

350

Ae. cylindrica Host sheds light on plasmon D evolution. Current Genetics 62:791–798.

351

https://link.springer.com/article/10.1007/s00294-016-0583-5

352

353

Hao M, Luo J, Zeng D, Zhang L, Ning S, Yuan Z, Yan Z, Zhang H, Zheng Y, Feuillet C,

354

et al. (2014) QTug.sau-3B is a major quantitative trait locus for wheat hexaploidization.

355

G3 Genes Genomes Genetics 4:1943–1953.

356

https://academic.oup.com/g3journal/article/4/10/1943/6025612

357

358

Harlan JR, deWet JMJ (1975) On Ö. Winge and a Prayer: The origins of polyploidy. The

359

Botanical Review 41:361–390

360

361

Hijmans RJ, Guarino L, Mathur P (2012) DIVA-GIS. http://www.diva-gis.org/Data.

362

Accessed 13 Mar 2022.

363

364

Kihara H (1944) Discovery of the DD-analyser, one of the ancestors of Triticum vulgare.

365

Agriculture and Horticulture 19:889–890. (in Japanese)

366

367

Kihara H (1946) Maturation division in F1 hybrids between Triticum dicoccoides ×

368

Aegilops squarrosa. La Kromosomo 1:6–11. (in Japanese with English summary)

11

369

370

Kihara H, Yamashita K, Tanaka M. (1965) Morphological, physiological, genetical and

371

cytological studies in Aegilops and Triticum collected from Pakistan, Afghanistan and Iran.

372

In: Yamashita K (ed) Results of the Kyoto University Scientific Expedition to the

373

Karakoram and Hindukush, 1955, Vol. I, Cultivated plants and their relatives. Kyoto

374

University, Kyoto, pp 1–118

375

376

Kilian B, Mammen K, Millet E, Sharma R, Graner A, Salamini F, Hammer K, Özkan H.

377

2011. Aegilops. In: Kole C (ed) Wild Crop Relatives: Genomic and Breeding Resources,

378

Cereals. Springer-Verlag, Berlin, pp 1–76

379

380

Korner-Nievergelt F, Roth T, von Felten S, Guelat J, Almasi B, Korner-Nievergelt P (2015)

381

Bayesian Data Analysis in Ecology using Linear Models with R, BUGS and Stan. Elsevier,

382

London

383

384

Kosambi DD. (1944) The estimation of map distance from recombination values. Annals

385

of Eugenics 12:172–175

386

387

Khoo KHP, Able AJ, Able JA (2012) Poor Homologous Synapsis 1 interacts with

388

chromatin but does not colocalise with ASYnapsis 1 during early meiosis in bread wheat.

389

International

390

https://downloads.hindawi.com/archive/2012/514398.pdf

Journal

of

Plant

Genomics

2012:514398.

391

392

Lenth RV (2016) Least-squares means: the R package lsmeans. Journal of Statistical

393

Software 69:1–33. https://www.jstatsoft.org/article/view/v069i01

394

395

Lloyd AH, Milligan AS, Langridge P, Able JA (2007) TaMSH7: a cereal mismatch repair

396

gene that affects fertility in transgenic barley (Hordeum vulgare L.) BMC Plant Biology

397

7:67. https://bmcplantbiol.biomedcentral.com/articles/10.1186/1471-2229-7-67

398

399

Matsuoka Y, Nasuda S, Ashida Y, Nitta M, Tsujimoto H, Takumi S, Kawahara T (2013)

400

Genetic basis for spontaneous hybrid genome doubling during allopolyploid speciation

401

of common wheat shown by natural variation analyses of the paternal species. PLoS

402

ONE

403

https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0068310

8:e68310.

404

12

405

Matsuoka Y, Takumi S, Kawahara T (2015) Intraspecific lineage divergence and its

406

association with reproductive trait change during species range expansion in central

407

Eurasian wild wheat Aegilops tauschii Coss. (Poaceae). BMC Evolutionary Biology 15:

408

213. https://bmcecolevol.biomedcentral.com/articles/10.1186/s12862-015-0496-9

409

410

Matsuoka Y, Mori N (2020) Reproductive and genetic roles of the maternal progenitor in

411

the origin of common wheat (Triticum aestivum L.). Ecology and Evolution 10: 13926–

412

13937. https://onlinelibrary.wiley.com/doi/full/10.1002/ece3.6985

413

414

Matsuoka Y, Nasuda S (2004) Durum wheat as a candidate for the unknown female

415

progenitor of bread wheat: an empirical study with a highly fertile F1 hybrid with Aegilops

416

tauschii

417

https://link.springer.com/article/10.1007/s00122-004-1806-6

Coss.

Theoretical

and

Applied

Genetics

109:

1710–1717.

418

419

Matsuoka Y, Takumi S (2017) The role of reproductive isolation in allopolyploid speciation

420

patterns: empirical insights from the progenitors of common wheat. Scientific Reports 7:

421

16004. https://www.nature.com/articles/s41598-017-15919-z

422

423

McFadden ES, Sears ER. 1944. The artificial synthesis of Triticum spelta. Records of the

424

Genetics Society of America 13:26–27

425

426

Mizuno N, Yamazaki M, Matsuoka Y, Kawahara T, Takumi S (2010) Population structure

427

of wild wheat D‐genome progenitor Aegilops tauschii Coss.: implications for

428

intraspecific lineage diversification and evolution of common wheat. Molecular Ecology

429

19: 999–1013. https://onlinelibrary.wiley.com/doi/10.1111/j.1365-294X.2010.04537.x

430

431

Nakagawa S, Schielzeth H. (2013) A general and simple method for obtaining R2 from

432

generalized linear mixed‐effects models. Methods in Ecology and Evolution 4: 133–142.

433

https://besjournals.onlinelibrary.wiley.com/doi/10.1111/j.2041-210x.2012.00261.x

434

435

R Core Team (2021) R: A language and environment for statistical computing. R

436

Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.

437

Accessed 5 October 2021

438

439

Röder MS, Korzun V, Wendehake K, Plaschke J, Tixier M-H, Leroy P, Ganal MW (1998)

440

Microsatellite

Map

of

Wheat.

13

Genetics

149:

2007–2023.

441

https://academic.oup.com/genetics/article/149/4/2007/6034278?login=true

442

443

Saisho D, Takumi S, Matsuoka Y (2016) Salt tolerance during germination and seedling

444

growth of wild wheat Aegilops tauschii and its impact on the species range expansion.

445

Scientific Reports 6: 38554. https://www.nature.com/articles/srep38554

446

447

Stacklies W, Redestig H, Scholz M, Walther D, Selbig J (2007) pcaMethods

448

Bioconductor package providing PCA methods for incomplete data. Bioinformatics 23:

449

1164-1167. https://academic.oup.com/bioinformatics/article/23/9/1164/272597

450

451

Takumi S, Naka Y, Morihiro H, Matsuoka Y (2009) Expression of morphological and

452

flowering time variation through allopolyploidization: an empirical study with 27 wheat

453

synthetics and their parental Aegilops tauschii accessions. Plant Breeding 128: 585–590.

454

https://onlinelibrary.wiley.com/doi/full/10.1111/j.1439-0523.2009.01630.x

455

456

Taylor J, Butler D. (2017) R package ASMap: efficient genetic linkage map construction

457

and

458

https://www.jstatsoft.org/article/view/v079i06

diagnosis.

Journal

of

Statistical

Software

79:

1–29.

459

460

van Slageren MW (1994) Wild wheats: a monograph of Aegilops L. and Amblyopyrum

461

(Jaub. & Spach) Eig (Poaceae). Wageningen Agricultural University, Wageningen

462

463

Wang J, Luo M-CC, Chen Z, You FM, Wei Y, Zheng Y, Dvorak J (2013) Aegilops tauschii

464

single nucleotide polymorphisms shed light on the origins of wheat D-genome genetic

465

diversity and pinpoint the geographic origin of hexaploid wheat. New Phytologist 198:

466

925–937. https://nph.onlinelibrary.wiley.com/doi/10.1111/nph.12164

467

468

Wickham H (2016) ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag, New

469

York

470

471

Wu Y, Bhat PR, Close TJ, Lonardi S (2008) Efficient and accurate construction of genetic

472

linkage maps from the minimum spanning tree of a graph. PLoS Genet. 4: e1000212.

473

https://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1000212

474

475

Statements and Declarations

476

Funding

14

477

This work was supported by the Japan Society for the Promotion of Science (JSPS)

478

KAKENHI Grant Numbers JP 20K20720, JP 19H02935, and JP 19KK0157.

479

480

Competing Interests

481

The author has no relevant financial or non-financial interests to disclose.

482

483

Author Contributions

484

The author contributed to the study conception and design, material preparation, data

485

collection, analysis, and draft writing.

486

487

Data Availability

488

The data that supports the findings of this study are available in the supporting

489

information of this article.

15

Table 1 Ae. tauschii accessions used and the estimated values for their ability to cause hybrid genome doubling

Estimated

value for the

No.

Accession

Lineage

Country of

origin

ability to

cause

Source a)

hybrid

Standard

Asymptotic lower

Asymptotic upper

error

confidence level

confidence level

genome

doubling

1 AE1090

TauL1

Kazakhstan

IPK

0.42

0.08

0.28

0.57

2 AT55

TauL1

China

OKAYAMA

0.23

0.06

0.14

0.36

3 AT76

TauL1

China

OKAYAMA

0.12

0.04

0.07

0.21

4 AT80

TauL1

China

OKAYAMA

0.24

0.06

0.14

0.38

5 IG126387

TauL1

Turkmenistan

ICARDA

0.31

0.08

0.18

0.48

6 IG127015

TauL1

Armenia

ICARDA

0.32

0.12

0.14

0.58

7 IG131606

TauL1

Kyrgyzstan

ICARDA

0.36

0.08

0.22

0.54

8 IG47259

TauL1

Syria

ICARDA

0.24

0.10

0.09

0.49

9 IG48042

TauL1

India

ICARDA

0.28

0.09

0.14

0.48

10 KU-2001

TauL1

Pakistan

KYOTO/NBRP

0.56

0.09

0.38

0.72

11 KU-2012

TauL1

Afghanistan

KYOTO/NBRP

0.37

0.09

0.21

0.56

12 KU-2025

TauL1

Afghanistan

KYOTO/NBRP

0.21

0.06

0.12

0.36

13 KU-2039

TauL1

Afghanistan

KYOTO/NBRP

0.46

0.09

0.30

0.64

16

14 KU-2068

TauL1

Iran

KYOTO/NBRP

0.08

0.05

0.02

0.25

15 KU-2132

TauL1

Turkey

KYOTO/NBRP

0.53

0.13

0.28

0.76

16 KU-2136

TauL1

Turkey

KYOTO/NBRP

0.40

0.13

0.19

0.65

17 KU-2144

TauL1

Iran

KYOTO/NBRP

0.32

0.07

0.20

0.48

18 KU-2816

TauL1

Armenia

KYOTO/NBRP

0.56

0.09

0.37

0.73

19 KU-2826

TauL1

Georgia

KYOTO/NBRP

0.49

0.12

0.27

0.72

20 KU-2828

TauL1

Georgia

KYOTO/NBRP

0.50

0.09

0.32

0.68

21 PI476874

TauL1

Afghanistan

USDA

0.29

0.07

0.18

0.43

22 PI486274

TauL1

Turkey

USDA

0.37

0.16

0.14

0.69

23 PI499262

TauL1

China

USDA

0.28

0.08

0.16

0.45

24 PI508262

TauL1

China

USDA

0.35

0.12

0.16

0.60

25 IG47202

TauL2

Azerbaijan

ICARDA

0.24

0.06

0.15

0.38

26 KU-20-10

TauL2

Iran

KYOTO/NBRP

0.34

0.08

0.20

0.52

27 KU-20-8

TauL2

Iran

KYOTO/NBRP

0.10

0.03

0.06

0.18

28 KU-20-9

TauL2

Iran

KYOTO/NBRP

0.40

0.08

0.26

0.55

29 KU-2069

TauL2

Iran

KYOTO/NBRP

0.13

0.06

0.06

0.28

30 KU-2074

TauL2

Iran

KYOTO/NBRP

0.35

0.09

0.20

0.54

31 KU-2075

TauL2

Iran

KYOTO/NBRP

0.30

0.08

0.18

0.47

32 KU-2076

TauL2

Iran

KYOTO/NBRP

0.33

0.07

0.21

0.47

33 KU-2078

TauL2

Iran

KYOTO/NBRP

0.48

0.09

0.32

0.65

34 KU-2079

TauL2

Iran

KYOTO/NBRP

0.25

0.06

0.15

0.37

17

35 KU-2080

TauL2

Iran

KYOTO/NBRP

0.04

0.01

0.02

0.08

36 KU-2088

TauL2

Iran

KYOTO/NBRP

0.47

0.08

0.32

0.62

37 KU-2090

TauL2

Iran

KYOTO/NBRP

0.29

0.07

0.17

0.45

38 KU-2091

TauL2

Iran

KYOTO/NBRP

0.30

0.09

0.16

0.50

39 KU-2092

TauL2

Iran

KYOTO/NBRP

0.54

0.08

0.39

0.69

40 KU-2093

TauL2

Iran

KYOTO/NBRP

0.34

0.07

0.21

0.48

41 KU-2096

TauL2

Iran

KYOTO/NBRP

0.24

0.07

0.13

0.39

42 KU-2097

TauL2

Iran

KYOTO/NBRP

0.05

0.02

0.03

0.09

43 KU-2098

TauL2

Iran

KYOTO/NBRP

0.20

0.05

0.12

0.33

44 KU-2100

TauL2

Iran

KYOTO/NBRP

0.46

0.10

0.29

0.65

45 KU-2103

TauL2

Iran

KYOTO/NBRP

0.58

0.08

0.43

0.72

46 KU-2104

TauL2

Iran

KYOTO/NBRP

0.57

0.08

0.41

0.73

47 KU-2105

TauL2

Iran

KYOTO/NBRP

0.38

0.08

0.25

0.54

48 KU-2106

TauL2

Iran

KYOTO/NBRP

0.39

0.08

0.25

0.54

49 KU-2109

TauL2

Iran

KYOTO/NBRP

0.32

0.12

0.14

0.58

50 KU-2111

TauL2

Iran

KYOTO/NBRP

0.51

0.12

0.29

0.72

51 KU-2124

TauL2

Iran

KYOTO/NBRP

0.14

0.05

0.07

0.26

52 KU-2126

TauL2

Iran

KYOTO/NBRP

0.24

0.10

0.09

0.49

53 KU-2155

TauL2

Iran

KYOTO/NBRP

0.18

0.06

0.09

0.33

54 KU-2156

TauL2

Iran

KYOTO/NBRP

0.30

0.07

0.18

0.45

55 KU-2158

TauL2

Iran

KYOTO/NBRP

0.39

0.07

0.26

0.54

18

a)

56 KU-2159

TauL2

Iran

KYOTO/NBRP

0.58

0.09

0.41

0.74

57 KU-2160

TauL2

Iran

KYOTO/NBRP

0.36

0.08

0.23

0.52

58 AE454

TauL3

Georgia

IPK

0.18

0.05

0.10

0.29

59 AE929

TauL3

Georgia

IPK

0.04

0.01

0.02

0.08

60 KU-2829A

TauL3

Georgia

KYOTO/NBRP

0.13

0.04

0.07

0.22

IPK, Institut für Pflanzengenetik und Kulturpflanzenforschung: ICARDA, International Center for Agricultural Research in the Dry Areas:

KYOTO, Plant Germ-plasm Institute of Kyoto University: NBRP, National BioResources Project: OKAYAMA, Kenji Kato, Okayama

University: USDA, U. S. Department of Agriculture.

19

Table 2 Summary of the values for the ability to cause hybrid genome doubling estimated

for the 60 Ae. tauschii accessions

Category

No. of accessions

Median

Mean

Standard deviation

Range

Overall

60

0.32

0.32

0.14

0.04–0.58

TauL1

24

0.34

0.35

0.13

0.08–0.56

TauL2

33

0.33

0.33

0.15

0.04–0.58

TauL3

0.13

0.11

0.07

0.04–0.18

20

Table 3 Additive multiple-QTL model a) for the ability to cause hybrid genome doubling in Ae. tauschii

QTL name

Chromosome

Position

LOD score

P b)

%var c)

(cM)

Estimated

Approximate

95%

Bayesian

effect

credible interval (cM) [flanking

(standard

marker name d)]

error)

2D@42.9

2D

42.9

8.34

0.00

9.3

-0.04 (0.01) 37.4 [6040147]

70.9 [12747359]

3D@54.3

3D

54.3

5.98

0.00

6.6

-0.03 (0.01) 43.7 [2257776]

59.4 [gwm52]

3D@105.8

3D

105.8

3.36

0.00

3.6

-0.02 (0.01) 94.2 [7345387]

140.3 [1106895]

6D@86.6

6D

86.6

3.34

0.00

3.6

-0.02 (0.01) 72.4 [1220491]

97.5 [1228345]

7D@161.0

7D

161.0

5.39

0.00

5.9

-0.03 (0.01) 142.7 [4540106]

164.8 [3955347]

a)

LOD score (relative to the no QTL model), %var by all terms in the model, and P-value based on the LOD score are 27.8, 36.8, and 0,

respectively.

b)

P denotes the drop-one-QTL-at-a-time analysis of variance P-values for the LOD peaks.

c)

%var denotes the estimated proportion of the phenotype variance that is explained.

d)

The numbers indicate the DArTseq maker IDs. The microsatellite marker gwm52 is described in Röder et al. (1998).

21

Figure Captions

Fig. 1

a Plot of the first two components from the probabilistic principal component analysis.

The first component PC1 (x) and second component (PC2) (y) account for 32.4% and

9.1% of the total variance, respectively. Circles, crosses, and squares indicate the TauL1,

TauL2, and TauL3 accessions, respectively. b Ae. tauschii lineage-wise box and dot plots

of the estimated ability to cause hybrid genome doubling

Fig. 2

Geographic patterns for the ability to cause hybrid genome doubling in Ae. tauschii.

Circles, crosses, and squares denote TauL1, TauL2, and TauL3, respectively. Each

accession is colored according to the ability value key. The three TauL1 accessions

(AT55, AT76, and AT80) from central China are not shown

Fig. 3

QTL analysis of the ability to cause hybrid genome doubling in Ae. tauschii. The

horizontal dashed line represents a significant LOD score determined by permutation

analysis

22

...