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Association between presence of Triticum timopheevii introgression and D-genome retention in hexaploid/tetraploid wheat crosses

Abstract

The 2G Triticum timopheevii introgression harbours genes for multiple disease resistance and quality traits in bread wheat. In order to transfer this segment from bread wheat into durum, the bread wheat line Sunguard, which carries this introgressed 2G segment was crossed with three tetraploid durum parents. A significant difference was observed in the segregation ratio of the 2G segment in the different crosses at the F2 generation with two of the three populations indicating segregation distortion against the hexaploid 2G segment. In these populations, the presence of the 2G segment was strongly correlated with the presence of D-genome chromosomes. These results were confirmed in the F4 generation of these populations. Six plants were identified in the F4 generation, which had retained the introgressed 2G segment in a homozygous condition and did not have a complete D-genome set. Two of these lines only had two non-homologous D-genome chromosomes in the F5 generation. Thus, the 2G segment and possibly other translocations can be transferred into durum wheat through hexaploid/tetraploid hybridisation.

Introduction

Discovering, developing and characterising novel sources of genetic variation for disease or pest resistances in wheat is a continuous process essential to maintaining crop health and sustaining productivity. Bread wheat (Triticum aestivum L.) and its related wheat species possess homologous or partly homologous genomes that harbour large beneficial allelic combinations for various disease resistances (Dundas et al. 2007). Several resistance genes that are effective against multiple pests and diseases have been introgressed into commercial bread wheat cultivars from wild relatives (Friebe et al. 1996; Molnár-Láng et al. 2015). There are a number of difficulties involved in the introgression of chromosomal segments from related and wild species into commercial wheat cultivars, such as genome compatibility and ploidy level. However, these difficulties can be overcome by selecting suitable breeding techniques and compatible genotypes (Jiang et al. 1993; Friebe et al. 1996).

A number of introgressions harbouring disease-resistance genes have been successfully deployed in bread wheat cultivars, and these have played a significant role in plant breeding for crop improvement and food security (Wulff and Moscou 2014). One example is the translocation of the tetraploid T. timopheevii (AtAtGG) segment on chromosome 2G to chromosome 2B in hexaploid wheat. This 2G introgression contains a number of desirable loci that confer resistance to stem rust (Olson et al. 2010; Bariana et al. 2001; Dundas et al. 2007), leaf rust (Leonova et al. 2007; Leonova et al. 2002), powdery mildew (Friebe et al. 1996; Tao et al. 2000), crown rot (Bovill et al. 2006) and black point (Lehmensiek et al. 2004). It also contains certain allelic combinations that are associated with improved grain quality characters, such as increased milling yield (Lehmensiek et al. 2006). A number of commercial Australian bread wheat varieties, including Sunco, Lang, Sunvale and Sunguard, possess this introgression (Friebe et al. 1996).

Alien introgressions have mainly been transferred from wild relatives into hexaploid wheat (Mago et al. 2005; Friebe et al. 1996). To our knowledge, only one study has reported on the transfer of an introgresssion from bread wheat into durum wheat (Martin et al. 2013). This study crossed Sunco with four different durum parents and found that the 2G introgression present in Sunco had not been transferred in two of the four crosses made. Detailed results with regard to the presence of 2G introgression in the remaining two populations were not presented and its presence in later generations was not investigated.

Developing pentaploid (AABBD, 5X) derived lines by crossing hexaploid (AABBDD, 6X) with tetraploid (AABB, 4X) wheat to transfer crown rot resistance into durum is one of the major foci of our research group (Eberhard et al. 2010; Martin et al. 2011; Martin et al. 2013; Padmanaban et al. 2017b). Our investigations have demonstrated wide variation between different pentaploid crosses both in the proportions of parental sequences inherited by the F2 A and B genomes and in the number of D chromosomes retained by the F2 generation (Padmanaban et al. 2017a).

This current study examines the transfer of the 2G segment from hexaploid Sunguard wheat, into a range of durum backgrounds. In particular, we have examined the proportion of F2 progeny which inherit the 2G segment, the retention of D-genome chromosomes in each of the crosses and the relationship between retention of the 2G segment and the retention of D-genome chromosomes in subsequent generations.

Materials and methods

Plant materials

Spring bread wheat, Sunguard (Sun289E/Sr2Janz), was crossed with spring durum wheat cultivars Caparoi (LY2.6.3/930054), Hyperno (Kalka sister line/Tamaroi) and WID802 (Syrica-1/Yallaroi//Tamaroi/Lingzhi/Yallaroi*2///RAC875/Kalka//Tamaroi////Lingzhi/Yallaroi//Tamaroi///Lingzhi/Yallaroi). Hexaploid/tetraploid crosses were developed in the glasshouse during 2014 following traditional hand emasculation and pollination (Riley and Chapman 1967). The F1 seeds from the pollinated heads were carefully collected and individually germinated in 24-well plates containing 2% water agar. One-week-old seedlings were transplanted to 200-mm-diameter plastic pots containing standard potting mixture (Searle’s® certified premium grade, Searle Pty. Ltd., Brisbane). The seedlings were grown in the glasshouse and F2 seeds were harvested at plant maturity.

DNA was extracted from individual 3-week-old F1 seedlings using a Wizard Genomic DNA purification kit (Promega Corporation, Sydney, Australia) as per the manufacturer’s instructions. Individually extracted F1 DNA samples were subjected to marker analysis to confirm their heterozygosity using selected microsatellite markers (cfa2278 and gwm345 on chromosome 2B) that showed polymorphism between the parents.

Microsatellite characterisation for the inheritance of the 2G segment and D-genome retention of F2 generation

Sixty randomly selected F2 seedlings were raised from each of the Sunguard/Caparoi, Sunguard/Hyperno and Sunguard/WID802 crosses. DNA was extracted from the 180 individual F2 plants and marker analysis was carried out to determine whether the 2G segment was present. Based on the consensus, molecular genetic map (Appels 2003) microsatellite primers on chromosome 2B that cover the complete introgressed 2G segment (cfa2278, gwm630, gwm319, wmc360, wmc441, and gwm501) were used. A set of 21 microsatellite primers (three for each of the seven non-homologous D chromosomes covering the long and short arms and the centromere region) were used to investigate the retention of D-genome chromosomes in the F2 plants (Padmanaban et al. 2017a). The same markers were used to investigate the retention of D-genome chromosomes in the F3 generation. Five randomly selected seeds from each of the 10 individually selected F2 plants were advanced to the F3 generation, i.e., 50 F3 lines for each of the three crosses. The 10 F2 families from each cross were chosen based on the D-genome content and the production of sufficient amount of viable seeds. D-genome content ranged from null to at least one copy of each of the seven non-homologous D chromosomes as indicated in Supplementary Table 1. F4 lines used in this study were obtained by selfing the F3 lines and advancing one seed of each plant.

Genome-wide DArTseq™ assay of F4 generation

Fifty lines of each of the Sunguard/Caparoi, Sunguard/Hyperno and Sunguard/WID802 crosses were investigated in the F4 generation using genome-wide DArTseq™ markers. DNA was extracted from 150 individual F4 lines using the CTAB method (Saghai-Maroof et al. 1984). The quality assessment and normalisation of DNA for the DArTseq™ assay were carried out as per Padmanaban et al. (2017). A hexaploid wheat microarray with the service tag DW16-2185 was used as a marker source.

Molecular and cytological validation in subsequent F5 generation

The presence of the 2G segment and D-genome retention in the subsequent F5 generation was analysed using microsatellite markers as described above. Rearranged D chromosomes identified in selected F4 lines were validated in the F5 generation using the genomic in situ hybridisation (GISH) technique. The cytological slide preparation and subsequent GISH were carried out as previously described (Zhang et al. 2004; Padmanaban et al. 2017b).

Statistical analysis

Differences in the inheritance of the 2G segment between crosses were assessed by performing a pairwise comparison test. The relationship between the D-genome retention and 2G inheritance in the F2 and F4 generation was tested using a Fisher’s test. A chi-square goodness of fit test was conducted to check the quality and segregation distortion of genome sequences developed through DArTseq™. Tukey’s post-hoc test was conducted to test the significant differences between the crosses by comparing the mean proportion of parental alleles in the A and B genomes and chromosomal 2G segment inheritance of F4 progeny. Statistical analysis was conducted using R software version 3.3.2 (R Development Core Team 2017) with multiple R packages including lme4 (Bates et al. 2014), lmerTest (Kuznetsova et al. 2017), multcomb (Hothorn et al. 2017), PMCMR (Pohlert 2014) and plyr (Wickham 2011).

Results

2G inheritance and D-genome retention in the F2 generation

Inheritance of the 2G segment and retention of D-genome chromosomes were investigated in 60 F2 lines from each of the crosses. Screening of these 180 F2 lines with microsatellite markers indicated significant differences in the segregation ratio of the 2G segment in different crosses (Table 1). A segregation ration of 1:2:1 (14:31:15) was observed for the Sunguard/Caparoi cross, whereas a significant distortion towards the durum parent (the absence of the 2G segment) was observed in the Sunguard/Hyperno (12:26:22) and Sunguard/WID802 (9:27:24) crosses.

Table 1 Segregation ratios of the 2G segment in 60 F2 lines of three crosses (2G+, homozygous for the 2G segment; H, heterozygous; 2G-, homozygous for the 2B segment from durum) are given together with an average and percentage of D-genome chromosomes retained in each cross

Significant differences (P < 0.05) were observed in the retention of D-genome chromosomes between the crosses (Table 1). D-genome chromosome numbers ranged from the presence of at least one copy of all seven non-homologous D-genome chromosomes (in 7, 17, and 5% of the lines of the Sunguard/Caparoi, Sunguard/Hyperno and Sunguard/WID802 crosses, respectively) to complete absence of D-genome chromosomes (in 10, 13, and 10% of the lines of the Sunguard/Caparoi, Sunguard/Hyperno and Sunguard/WID802 crosses, respectively).

Relationship between 2G inheritance and D-genome retention

A strong correlation (P < 0.001) was observed between the 2G segment and the number of D-genome chromosomes retained in the three crosses (Fig. 1). Lines that were homozygous for the 2G segment retained between four and seven non-homologous D-genome chromosomes, while the lines that were homozygous for the tetraploid 2B chromosomal segment in all but one case possessed less than four non-homologous D-genome chromosomes (Fig. 1).

Fig. 1
figure1

Relationship between the inheritance of the 2G segment and the retention of D-genome chromosomes in 60 F2 progeny from each of the three crosses (a Sunguard/Caparoi, b Sunguard/Hyperno, c Sunguard/WID802). 2G+ lines are homozygous for the 2G segment and 2G- lines are homozygous for the 2B segment from durum

Detection of 2G segment in F4 generation

To determine the presence of the 2G introgression in F4 lines, 1094 unique polymorphic DArT sequences on chromosome 2B were utilised. The introgressed 2G segment was located between 59 and 103 cM, which is approximately 42 cM in length according to the map supplied by DArT Pty Ltd.

The 2G segment, which was present in 21 of the 30 lines that were investigated in the F2 generation (of which 13 were heterozygous and eight homozygous for the 2G introgression), was present in only eight of the 30 families (27%) in the F4 generation (Table 2). The 13 lines that were heterozygous for the 2G segment in the F2 generation had lost the 2G segment and were homozyogus for the durum 2B segment in the F4 generation. No recombinations were detected within the 2G segment suggesting that the introgression was transferred as a whole segment.

Table 2 Number of D-genome chromosomes retained in 10 F4 families of each of the Sunguard crosses. Each row represents an individual line and each column represents a non-homologous D chromosome. Red and yellow colors represent the presence and absence of D chromosomes, respectively. Inheritance of the 2G segment for each Sunguard cross is given with A and B indicating the presence and absence of the 2G segment, respectively. Lines highlighted in the Sunguard/Caparoi cross were advanced to the F5 generation. Incomplete chromosomes are highlighted in green

Most of the lines of the F4 generation either had a complete durum set of chromosomes (2n = 4× = 28) or had at least one copy of each of the seven non-homologous D chromosomes (Table 2). Only two out of 50 lines from the Sunguard/Hyperno cross retained at least one copy of each of the seven D chromosomes. Fifty and 40% of the Sunguard/Caparoi and Sunguard/WID802 F4 families, respectively, had lost the D-genome chromosomes completely (Table 2).

Rearranged D chromosomes were observed in eight of 150 F4 progenies, three from the Sunguard/Caparoi and five from the Sunguard/Hyperno cross (Table 2). Cytological tests were conducted on six of these F5 lines (7.1, 37.1 and 37.2 from the Sunguard/Caparoi cross and 39.5, 44.1 and 44.5 from the Sunguard/Hyperno cross). GISH results confirmed the presence of telocentric chromosomes in lines 7.1, 37.1 and 37.2 (Fig. 2). A pair of whole arm translocations between A and B chromosomes and a single telocentric 3DL with intact centromere were observed in line 39.5. Furthermore, translocations were observed between A and D chromosomes in lines 44.4 and 44.5. Both of these lines possessed a stable durum set of chromosomes (2n = × 4 = 28) with a 2DS segment translocated onto an A-genome chromosome (Fig. 2).

Association of introgressed 2G segment with D-genome chromosomes

A Fisher’s test was conducted to confirm that there was still a strong correlation (P < 0.001) between the introgressed 2G segment and the retention of D-genome chromosomes in the F4 generation (Figs. 3). Only six of the 40 lines that inherited the 2G segment did not have a full set of D-genome chromosomes (Table 2). Three of these lines produced viable seeds and were advanced to the F5 generation (Supplementary Table 2). Marker analysis of the F5 generation confirmed that the 2G segment was present in a homozygous status in all of these lines. The dominant marker gwm501 positioned at the distal end of the 2G segment was absent in two of the lines (Supplementary Table 2). Three lines were identified which had retained only two (chromosomes 3D and 7D and 4D and 6D, respectively) or three D-genome chromosomes (1D, 5D and 6D).

Fig. 2
figure2

Multi-coloured GISH analyses of rearranged D chromosomes in selected F5 lines of the Sunguard/Caparoi and Sunguard/Hyperno crosses. a Line number 6.5 with arrow indicating a telocentric 3DL chromosome. b Stable durum line number 7.4 with 2DS segment translocated to a pair of A-genome chromosomes (indicated by arrows). A-genome chromosomes are green, B-genome chromosomes are blue and D-genome chromosomes are pink in colour

Fig. 3
figure3

Relationship between the inheritances of 2G segment and the retention of D-genome chromosomes in 150 F4 lines; 2G+ lines are homozygous for the 2G segment and 2G-lines are homozygous for the 2B segment from durum

Discussion

Three sets of crosses were developed to investigate the presence of the T. timopheevii 2G segment in the progeny of inter-ploidy crosses. Sunguard, a current commercial bread wheat variety, which harbours the 2G segment was used as the maternal parent to cross with three different durum varieties. Differences were observed between the crosses in the segregation ratios of the 2G segment with only the Sunguard/Caparoi cross segregating in the expected 3:1 ratio for the 2G segment. In the Sunguard/Hyperno and Sunguard/WID802 crosses, segregation distortion towards the durum chromosome 2B was observed.

The DArT analysis of the subsequent F4 generation confirmed preferential retention of the durum chromosome 2B with all heterozygous F2 lines having become homozygous for the durum 2B chromosome in the F4 generation. These results differ from previous reports on hexaploid/hexaploid wheat crosses, where one parent possesses the 2G segment. In these crosses, a significant segregation distortion towards the retention of the 2G segment was observed (Kammholz et al. 2001; Kammholz et al. 1998; Bovill et al. 2006; Bovill et al. 2010).

Lines homozygous for the 2G segment had retained a large number of D-genome chromosomes ranging from four to seven. The F2 lines that were heterozygous for the 2G segment had an intermediate D-genome number ranging from three to six. This suggests that hexaploid/tetraploid derived lines, which have eliminated the durum 2B segment and retained the 2G segment, may need to be compensated by retaining a large number of D-genome chromosomes. DArT analysis in the advanced F4 population confirmed that there is a strong relationship between the introgressed 2G segment and D-genome retention, which suggests that it may be difficult to introduce the 2G segment into a tetraploid durum background. Whether this D-genome association is only occurring with the 2G introgression or also with other bread wheat introgressions needs to be further investigated.

The 2G segment was transmitted as a whole without any chromosomal cross-overs. This is similar to another study, where the translocation was transferred between bread wheats as a whole segment (Lehmensiek et al. 2005). Using Sunguard as the donor parent to introduce the 2G segment into durum may not be ideal as only a small number of progeny segregated for the 2G segment and most of these lines had a full set of D-genome chromosomes. Other 2G donors should be tested to determine whether this is the same with all 2G donors. However, in a previous study using bread wheat Sunco as the 2G donor parent, the 2G segment was not transferred to the progeny in two of the four Sunco/durum crosses (Martin et al. 2013). The pedigrees of Sunguard (Sun289E/Sr2Janz) and Sunco (SUN9E27*4/3AG14//WW15/3/3*COOK) are different, suggesting that the transfer of the 2G segment into durum is not strongly influenced by the maternal parent.

Six F4 lines from the Sunguard/Caparoi and Sunguard/Hyperno crosses had inherited the 2G segment and did not have a full set of D-genome chromosomes. Because these lines did not retain complete D-genome sets, there is a high chance of D chromosomes being eliminated in future generations. Unfortunately, viable seed could only be obtained from three of these lines. They will be screened for crown rot resistance in the near future and may be of interest to durum breeding programs as they may also contain other useful traits.

Similar to previous studies, telocentric chromosomes with intact centromeres were observed in a number of F5 lines (Koo et al. 2015; Padmanaban et al. 2018). The present study also validated two durum lines from the Sunguard/Hyperno cross with 2DS translocated to an A-genome chromosome. These lines with an extra 2DS segment may have traits which could be potentially useful for durum breeding in future.

To obtain tetraploid durum lines (2n=4X=28) containing the 2G segment further selfing of F5 lines that were homozygous for the 2G segment and only had four or less non-homologous D-genome chromosomes may need to be undertaken to eliminate remaining D chromosomes. However, a previous study has indicated that paired D-chromosomes may become stable in later generations (Padmanaban et al. 2018). Backcrossing with the durum parent may be another approach to eliminate remaining D chromosomes; however, this could result in the loss of the 2G translocation. An alternative option is to cross F5 lines that are homozygous for the 2G segment and have different copies of D-genome chromosomes. The progenies derived from these crosses are likely to inherit any single non-homologous D chromosome, which may be eliminated in subsequent generations of selfing. Irrespective of which strategy is chosen to obtain tetraploid lines large-sized populations need to be developed to increase the chances of obtaining lines, which have the introgression and a low number of or no D chromosomes. Overall, this study has shown that the 2G segment and possibly other alien translocations can be transferred to the durum wheat background through hexaploid/tetraploid wheat crosses; however, different strategies may need to be considered for the elimination of D-genome chromosomes.

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Funding

This study was partly funded by the Grain Research and Development Corporation, Australia. An Australian Postgraduate Award supported Sriram Padmanaban’s Ph.D. study.

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Correspondence to Anke Martin.

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Electronic supplementary material

Supplementary Table 1

Retention of D-genome chromosomes in 180 F2 progeny of three crosses. Each row represents an individual line and each column represents a non-homologous D chromosome. Red and yellow colours indicate the presence and absence of D chromosomes, respectively. Highlighted lines from each cross were advanced to the F4 generation. Inheritance of the 2G segment in each of the crosses is shown (A = maternal, H = heterozygous and B = paternal genotype) (DOCX 57 kb)

Supplementary Table 2

Microsatellite markers amplified across 2G segment of 26 selected F5 progeny of the Sunguard/Caparoi cross (A = maternal and B = paternal genotype). The estimated locations of the microsatellite markers on chromosome 2B according to consensus map by Apples (2003) are indicated. The number of D chromosomes retained in each of the 26 F5 lines is also given (DOCX 15 kb)

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Padmanaban, S., Zhang, P., Sutherland, M.W. et al. Association between presence of Triticum timopheevii introgression and D-genome retention in hexaploid/tetraploid wheat crosses. Mol Breeding 38, 84 (2018). https://doi.org/10.1007/s11032-018-0838-6

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Keywords

  • 2G introgression
  • Inter-ploidy crosses
  • Wheat breeding
  • T. timopheevii 2G