Elsevier

Plant Science

Volume 285, August 2019, Pages 193-199
Plant Science

Wheat domestication in light of haplotype analyses of the Brittle rachis 1 genes (BTR1-A and BTR1-B)

https://doi.org/10.1016/j.plantsci.2019.05.012Get rights and content

Highlights

  • Wheat carry mutations in the BTR1-A and BTR1-B genes affecting spike shattering.

  • We probed the geographical provenances of these mutations via haplotype analyses.

  • The progenitor haplotypes were identified in a collection of wild wheat accessions.

  • A single Southern Levant accession harbored both BTR1 progenitor haplotypes.

  • This imply that Southern Levant played an important role in wheat domestication.

Abstract

Wheat domestication was a milestone in the rise of agrarian societies in the Fertile Crescent. As opposed to the freely dispersing seeds of its tetraploid progenitor wild emmer, the hallmark trait of domesticated wheat is intact, harvestable spikes. During domestication, wheat acquired recessive loss-of-function mutations in the Brittle Rachis 1 genes, both in the A genome (BTR1-A) and B genome (BTR1-B). In this study, we probe the geographical provenances of these mutations via haplotype analyses of a collection of wild and domesticated accessions. Our results show that the precursor of the domesticated haplotype of BTR1-A was detected in 32% of the wild accessions gathered throughout the Levant, from central Israel to central Turkey. In contrast, the precursor of the domesticated haplotype of BTR1-B, which carries a distinct 11 bp deletion in the promoter region, was found in only 10% of the tested wild accessions, all from the Southern Levant. Moreover, we identified of a single wild emmer accession in Southern Levant that carries the progenitor haplotypes for both BTR1-A and BTR1-B genes. These observations suggest that at least part of the emmer domestication process occurred in Southern Levant, contrary to the widely held view that the northern part of the Fertile Crescent was the center of wheat domestication.

Introduction

Wheat (Triticum spp.) was domesticated ˜10,000 years ago in the Near-Eastern Fertile Crescent and is one of the Neolithic founder crops [1]. Tetraploid wheat domestication was initiated by genetic modifications of wild emmer wheat (WEW; T. turgidum ssp. dicoccoides (Körn.) Thell.; genome BBAA). The product of the WEW domestication was domesticated emmer wheat (DEW; T. turgidum ssp. dicoccum Schrank), from which evolved Durum wheat (T. turgidum ssp. Durum (Desf.) MacKey) and other free-threshing forms of tetraploid wheat [2]. Subsequently, hexaploid bread wheat (T. aestivum L., genome BBAADD) arose from the hybridization of domesticated tetraploid wheat with the diploid Aegilops tauschii Coss. (genome DD) [3]. Diploid einkorn wheat T. monococcum subsp. monococcum (2n = 2x = 14, AmAm), which is nowadays a minor crop, was independently domesticated from its wild progenitor T. monococcum L. subsp. boeoticum (Boiss.) Á. Löve et D. Löve [4].

Crop domestication is marked by modification of key traits, referred to as the domestication syndrome, which is followed by subsequent evolution introducing further incremental changes in morpho-physiological traits [[5], [6], [7]]. Cereal domestication syndrome involves traits primarily related to spike morphology, seed development, and seed dormancy. The most conspicuous difference between domesticated cereals and their wild progenitors is spike disarticulation. The spikes of wild cereals shatter at maturity (brittle rachis, BR trait) while those of domesticated cereals remain intact (non-BR trait), enabling easier harvest [8,9]. Non-brittle rachis is therefore considered to be the diagnostic indicator of domesticated cereals. Evolution of DEW with non-brittle spikes, which was the dominant cereal in the Middle East for nearly five millennia, is a classic example of this process.

Genetic analysis in Triticeae have revealed several loci affecting BR on homologous chromosomes 2, 3, 4 and 5 [6,[10], [11], [12], [13], [14]]. In barley, the brittle rachis trait is conditioned by the allelic status at two physically linked genes on chromosome 3H, Brittle rachis 1 (BTR1) and Brittle rachis 2 (BTR2). A loss-of-function in either gene results in non-brittle spikes. Loss-of-function mutations in both genes are found in the domesticated barley genepool, implying at least three independent origins of the non-brittle rachis phenotype in barley [15,16]. While both BTR1 and BTR2 were detected on wheat chromosomes 3A and 3B, only mutations in BTR1 are responsible for non-shattering spikes in domesticated einkorn, emmer, Durum, and bread wheat [4,11].

Understanding the genetic architecture of the domesticated phenotype in wheat answers ‘how’ non-shattering evolved but not ‘where’. Recently, tracing BTR1 haplotype variation back to wild einkorn samples provided evidence that the einkorn progenitor came from the Kartal–Karadağ Mountains in Eastern Turkey. Further to the east, the area between Gaziantep and the Karadağ mountains, was also shown to harbor the immediate wild ancestors of the btr2 [15] and btr1b [16] lineages of domesticated barley. These congruent results lend support to the ‘Cradle of Agriculture’ hypothesis, which suggests the northern part of the Fertile Crescent was the site of domestication of all seven Neolithic founder crops [1].

Here, we use the sequence of wild emmer [11] to define haplotypes for BTR1-A and BTR1-B genes, the orthologs of the barley BTR1 gene, on wheat-chromosomes 3A and 3B, respectively. We then re-sequence the haplotypes in a strategically selected group of accession of wild and domesticated wheats with the goal of identifying haplotypes in WEW gene pool that are the progenitor haplotypes of those present in domesticated wheat. We then use the geographic distribution of progenitor haplotypes to identify the most likely area of emmer domestication.

Section snippets

Core collections

The primary Core collection for this study included 33 WEW, 28 DEW, 8 Durum and 5 bread wheat accessions (Table S1). The genomic diversity of most of the WEW and DEW genotypes in this collection was characterized previously using a whole exome capture assay [11]. The secondary Core collection had 377 wild and 81 domesticated accessions (Table S7), including accessions in the primary collection and an additional 279 WEW accessions from Southern Levant, 70 WEW accessions from Turkey (Northern

BTR1-A haplotype analysis

To find the origin of the domesticated, non-shattering btr1-A allele, we re-sequenced a 2254 bp region (Zavitan v.1, chr. 3A 61,638,576 – 61,640,829) that includes the 591 bp BTR1-A coding region along with 751 bp upstream and 912 bp downstream sequences. In addition to a 2-bp frameshift deletion within the coding sequence, which separates wild from domesticated wheat [11], our sequence analysis identified 10 SNPs, all located downstream of the BTR1-A coding region (Fig. 1a, File S1). Together,

Discussion

Our haplotype analysis of the wheat domestication gene BTR1-A revealed that the 2-bp deletion responsible for the non-BR phenotype [11] has a monophyletic origin. Further genetic analysis of a 15 kbp region surrounding this gene confirmed the close relationship between domesticated haplotype BTR1-A-hap11 and founder haplotype BTR1-A-hap10.

WEW is divided into northern and southern subpopulations [20,21]. Haplotype BTR1-A-hap10, widely distributed throughout the Northern and Southern Levant, is

Author contribution

Conceptualization and supervision, A.D.; investigation, M.N.; resources, H.S., E.Ç. and H.O.; writing—original draft preparation, A.D., I.H. and M.N.; writing—review and editing, all authors; visualization, R.A.

Acknowledgements

This research was funded by the United States – Israel Binational Science Foundation (BSF grant 2015409), the US-Israel Binational Agricultural Research and Development Fund (BARD project No. IS-4829-15), and the Israel Science Foundation (ISF grant 1137/17). HO acknowledges support from Çukurova University (FBA-2017-7930).

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