PLOS ONE
RESEARCH ARTICLE
Identification of a novel stripe rust resistance
gene from the European winter wheat cultivar
‘Acienda’: A step towards rust proofing wheat
cultivation
Gomti Grover 1
I *, Achla Sharma 1
D ID , Ian Mackay 2
ID , Puja Srivastava1, Satinder Kaur1,
Jaspal Kaur1, Amanda Burridge 3
ID , Sacha Przewieslik Allen3, Alison R. Bentley 4¤
ID ,
Parveen Chhuneja 1
ID , N. S. Bains1
1 Punjab Agricultural University, Ludhiana, India, 2 IMPlant Consultancy Ltd., Chelmsford, United Kingdom,
3 Life Sciences, University of Bristol, Bristol, United Kingdom, 4 The John Bingham Laboratory, NIAB,
a1111111111 Cambridge, United Kingdom
a1111111111
a1111111111 ¤ Current address: International Maize and Wheat Improvement Center (CIMMYT), Texcoco, Mexico
* gomtigrover@pau.edu
a1111111111
a1111111111
Abstract
All stage resistance to stripe rust races prevalent in India was investigated in the European
OPEN ACCESS winter wheat cultivar ‘Acienda’. In order to dissect the genetic basis of the resistance, a
Citation: Grover G, Sharma A, Mackay I, Srivastava backcross population was developed between ‘Acienda’ and the stripe rust susceptible
P, Kaur S, Kaur J, et al. (2022) Identification of a Indian spring wheat cultivar ‘HD 2967’. Inheritance studies revealed segregation for a domi-
novel stripe rust resistance gene from the
nant resistant gene. High density SNP genotyping was used to map stripe rust resistance
European winter wheat cultivar ‘Acienda’: A step
towards rust proofing wheat cultivation. PLoS ONE and marker regression analysis located stripe rust resistance to the distal end of wheat chro-
17(2): e0264027. https://doi.org/10.1371/journal. mosome 1A. Interval mapping located this region between the SNP markers AX-95162217
pone.0264027 and AX-94540853, at a LOD score of 15.83 with a phenotypic contribution of 60%. This
Editor: Dragan Perovic, Julius Kuhn-Institut, major stripe rust resistance locus from ‘Acienda’ has been temporarily designated as Yraci.
GERMANY A candidate gene search in the 2.76 Mb region carrying Yraci on chromosome 1A identified
Received: September 21, 2021 18 NBS-LRR genes based on wheat RefSeqv1.0 annotations. Our results indicate that as
Accepted: January 31, 2022 there is no major gene reported in the Yraci chromosome region, it is likely to be a novel
stripe rust resistance locus and offers potential for deployment, using the identified markers,
Published: February 16, 2022
to confer all stage stripe rust resistance.
Copyright: © 2022 Grover et al. This is an open
access article distributed under the terms of the
Creative Commons Attribution License, which
permits unrestricted use, distribution, and
reproduction in any medium, provided the original
author and source are credited.
Introduction
Data Availability Statement: All relevant data are
within the manuscript and its Supporting Global wheat demand is projected to rise at an annual rate of 1.6% to 2050 on account of
Information files. increasing population and income levels [1]. Wheat is vulnerable to a number of biotic and
Funding: The author(s) received no specific abiotic stresses depending on the agro-climatic zones. Stripe rust caused by Puccinia striiformis
funding for this work. f. sp. tritici, (Pst) is an economically important foliar disease prevalent in all major wheat grow-
Competing interests: The authors have declared ing regions and considered the most destructive disease of wheat throughout the world [2]. It
that no competing interests exist. poses a significant threat to wheat productivity, leading to significant yield losses.
PLOS ONE | https://doi.org/10.1371/journal.pone.0264027 February 16, 2022 1 / 8
PLOS ONE Novel stripe rust resistance gene from the wheat cultivar ‘Acienda’
Historically stripe rust has caused epidemics in cool and moist regions, but it is now more
frequently reported in warmer and drier areas suggesting an expansion in its range of adapta-
tion [3–6]. Its increasing importance as a destructive wheat pathogen is also likely due to con-
tinuous evolution of new virulences [7]. A recent study estimated that 88% of the world’s
wheat production is now prone to stripe rust infection, resulting in global losses of at least 5
million tonnes annually [6].
Stripe rust can be controlled by the application of fungicides but this increases the costs of
wheat production and can be ineffective if not applied at correct time [8]. The widespread use
of fungicides also leads to negative environmental effects due to chemical residues. Therefore,
there is a clear need to focus on deploying and updating genetic resistance in wheat varieties
against evolving stripe rust races. Characterisation of genetic resistance for stripe rust was first
described in the wheat cultivar Rivet [9] and remains an active process in global wheat research
[10, 11]. Currently, more than 70 stripe rust resistance genes, designated through Yr1 to Yr76,
have been catalogued in different hexaploid bread, durum wheat, and wild species back-
grounds [11]. However, progress in the discovery and introgression of novel genes and alleles
is typically hampered by the availability of identified donor stocks with proven resistances, the
long time frames necessary for identifying even monogenic resistances, and the disconnect
between gene identification and mobilization in breeding. Biotechnological approaches help
in elucidating the molecular mechanism of resistance. With the advent of DNA-based molecu-
lar markers, plant breeding with the aid of marker assisted selection (MAS) has given new
dimensions to crop improvement. Characterization of genes and identification of linked
molecular markers are powerful tools in deployment of desirable traits into elite background.
A single dominant stripe rust resistance source in the European bread wheat cultivar
‘Acienda’ was reported in our previous report [12]. In the present study, we report molecular
mapping of this all-stage stripe rust resistance gene using high throughput SNP genotyping in
backcross populations. This new gene offers an additional source of stripe rust resistance sup-
porting the breeding of future disease resistant wheat cultivars.
Results
Phenotypic analysis indicates monogenic control of stripe rust resistance
Both BC1F2 populations conformed to a segregation ratio of 3 resistant (R) to 1 susceptible(S)
(3R:1S), indicating a single dominant stripe rust resistance locusfrom Acienda (Table 1). Prog-
eny test in BC1F3 showed segregation in a 1:2:1 ratio again confirming dominant monogenic
inheritance (Table 1).
Molecular mapping confirms presence of a major resistance locus on
chromosome 1A
Out of 35,143 SNP markers of wheat breeders’ array, 2,359 polymorphic SNP markers were
used for mapping stripe rust resistance at BC1F3. Detail of filtering of 35K SNP markers were
Table 1. Segregation and chi-square analysis of resistance in BC1F2 plants and BC1F3 progeny indicates segregation of single dominant locus.
Population @ No. of BC1F2 plants No. of BC1F3 progeny#
Resistant Susceptible χ2 (3:1) HR Seg. HS χ2 (1:2:1)
P1 68 18 0.76 22 46 18 0.79
P2 88 18 3.64 28 56 18 2.94
@derived from two BC1F1 plants
#HR: homozygous resistant; Seg: segregating; HS: homozygous susceptible.
https://doi.org/10.1371/journal.pone.0264027.t001
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PLOS ONE Novel stripe rust resistance gene from the wheat cultivar ‘Acienda’
Fig 1. (a) Genome wide marker trait associations for stripe rust resistance in Acienda/HD2967 BC1F3 population
generated in R/qtl showing a single large peak on chromosome 1A. (b) LOD scores for chromosome 1A depicting
mapping of Yraci (c) Mapping of stripe rust resistance in Acienda/HD2967 population on wheat chromosome 1A
using ICI Mapping software. Physical locations of the markers are indicated in Mb.
https://doi.org/10.1371/journal.pone.0264027.g001
described in material method section. These 2359 markers were distributed across all 21 wheat
chromosomes as summarised in S1 Table in S1 File. Marker regression analysis was performed
using the Haley-Knott method as implemented in R/qtl. This detected one prominent peak on
chromosome 1A flanked by SNP marker AX-95162217 at a LOD score of 11.4 (Fig 1A). Two
minor peaks were also observed on chromosome 2A but these were below the LOD threshold
(3.5 and 3.0, respectively) and were not considered further. Some markers which could not be
assigned to any of the linkage groups remained unmapped.
Single marker analysis (SMA) was also performed using the ICI mapping which confirmed
the mapping of stripe rust resistance in the interval flanked by SNP markers AX-94540853 and
AX-95162217 at a LOD score of 16.99. Interval mapping with ICIM detected major QTL
flanked by SNP markers AX-95162217 and AX-94540853 with a LOD score of 15.83 explain-
ing 60% of the phenotypic variation (Fig 1C). Based on the existing consensus genetic map
(Allen et al. 2017), AX-95162217 and AX-94540853 were mapped in the bin at 54.04cM on
chromosome 1A. This new stripe rust resistance locus on 1A is designated as Yraci.
Physical locations of the SNP markers linked to Yraci were obtained by BLAST search
against the IWGSC Ref Seq v1 genome assembly (IWGSC, 2018). A physical interval of 2.76
Mb between markers AX-95162217 (3.76Mb) and AX-94540853 (6.52Mb) defined the position
of Yraci. Candidate genes in this 2.76 Mb region harbouring Yraci, were identified from
IWGSC Ref Seq v1.0 annotation which revealed a total of 18 NBS-LRR genes in this region (S2
Table in S1 File).
Discussion
In this study we report the phenotypic and genetic characterisation of a stripe rust resistance
locus Yraci from the European winter wheat cultivar ‘Acienda’. Analysis of segregation pat-
terns of resistance in backcross populations developed from ‘Acienda’ and the Indian spring
wheat ‘HD 2967’ support monogenic inheritance of the locus, confirming the previous find-
ings in [12]. Genotyping the backcross population with the high-density 35K Affymetrix
Wheat Breeders SNP array produced 2,359 informative markers for mapping. The low number
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PLOS ONE Novel stripe rust resistance gene from the wheat cultivar ‘Acienda’
of polymorphic markers identified for the population most likely reflected the backcross
derived nature of the material used in the study. The backcross with ‘HD2967’ was primarily
performed for mobilization of resistance into the elite and adapted agronomic background.
Moreover, the synchronization of the phenological stages for uniform disease evaluation could
also be achieved to ensure uniform disease evaluation.
Genetic characterization identified a single locus on chromosome 1A explaining 60% of the
phenotypic variation in resistance. This was assigned as the stripe rust resistance locus Yraci
located in a 2.76 Mb interval between SNP markers AX-95162217 and AX-94540853 on the
distal end of chromosome 1A. No major stripe rust resistance gene has been previously
reported in this region although previous studies have detected minor quantitative trait loci
(QTL). Based on reports in literature, ‘Janz’, an Australian cultivar susceptible to Pst isolates at
the seedling stage showed an adult plant stripe rust resistance response [13] which was mapped
to a minor QTL from ‘Janz’ on chromosome 1A, explaining 6–7% of the phenotypic variation
and designated as QYr.sun-1A. A minor QTL on 1A (QYrid.ui-1A) responsible for high-tem-
perature adult-plant resistance to stripe rust has also been reported from the resistant source
‘IDO444’ [14]. A further QTL (QYr.tam-1AS) derived from ‘TAM 111’, a hard red winter
wheat cultivar resistant to Pst races in the southern-central USA was reported to be located on
1AS chromosome of wheat, explaining 17% phenotypic variation [15]. These previous putative
stripe rust resistance loci indicate that minor QTLs for adult plant resistance reside on chro-
mosome 1A chromosome. The mapping of a major effect all stage resistance locus on chromo-
some 1A in this study suggests that Yraci is a novel resistance source that has not yet been
exploited for spring wheat improvement.
The available Ref Seq v1.0 wheat genome annotation (IWGSC, 2018) allowed the identifica-
tion of 18 candidate NBS-LRR family genes in the mapped interval. Disease resistance genes
are typically found in clusters and use of physical distance (rather than genetic distance) per-
mitted the narrowing of the region. Further work is required to develop markers for character-
ising and tracking these specific gene for use in resistance breeding. This is crucial as
accelerated evolution of stripe rust pathotypes have been reported in India. The appearance of
race 78S84 which has virulence for Yr27 [16] broke down the resistance of ‘PBW343’, a cultivar
widespread in India for over a decade (1995–2007). In addition, two newly evolved pathotypes
(110S119 first reported in 2014 from Ropar, Punjab, India; 238S119 first reported in 2014
from Himachal Pradesh, India) have led to the breakdown of resistance in breeding pipelines
as well in the cultivars released after ‘PBW343’ [17, 18].
This catalysed wheat breeders and wheat pathologists to mobilise known gene resistance
into agronomically acceptable backgrounds and also to identify novel sources of resistance to
be used in future. Currently, resistance breeding depends on a relatively small number of resis-
tance genes (Yr5, Yr10, Yr15, Lr37/Yr17 and Lr76/Yr70) which are being used in various, but
often limited. combinations. This limitation presents an urgent need to diversify the available
resistant sources. We demonstrate that Yraci is a new locus offering additional support to
wheat breeders for developing durable stripe rust resistance.
The European winter wheat variety Acienda was registered in France in 2004 and postu-
lated to have Lr13 leaf rust resistant gene [19]. Leaf rust is the major foliar disease of wheat in
France, and by 2007 the majority of French cultivars had two (Lr13, Lr37) or three (Lr10, Lr13,
Lr37) gene combinations. In India, Acienda showed strong resistance to all prevalent stripe
rust races and pathotypes in field screening experiments. Further, it did not show presence of
other effective stripe rust resistance genes currently in use in India when screened with avail-
able linked molecular markers [12]. Via backcross introgression into an agronomically elite
Indian spring wheat background we mapped the novel Yraci locus to chromosome 1A and cre-
ated advanced germplasm carrying the locus for use in breeding. This represents a new source
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PLOS ONE Novel stripe rust resistance gene from the wheat cultivar ‘Acienda’
of stripe rust resistance for the region and the germplasm developed is an important resource
for future wheat breeding and improvement.
Materials and methods
Plant material
The European winter wheat cultivar ‘Acienda’ was identified as having all stage stripe rust
resistance in field trials at Punjab Agricultural University (PAU), Ludhiana, India (30˚ 54’ N
latitude, 75˚ 48’ E longitude, and 247m above m s l) over five seasons (2011–2016) [12]. The
resistant donor parent ‘Acienda’ was selected from the 376-line European winter wheat Triti-
ceae Genome association mapping panel [20]. ‘Acienda’(Tremie/Sideral), is a cultivar with
winter growth habit that was released in France in 2004 and was widely grown [19, 21]. In
order to map the resistance, ‘Acienda’ was crossed with stripe rust susceptible spring wheat
cultivar, ‘HD 2967’ and the F1 plants backcrossed to ‘HD 2967’. Wheat variety ‘HD2967’ is cur-
rently the most widely grown cultivar (based on seed production) in India [18]. The BC1F1
plants were screened for stripe rust under artificial epiphytotic conditions in the field and
resistant BC1F1 plants were individually harvested. Further the individual BC1F2 seeds were
space planted in the field and screened for stripe rust resistance. Two BC1F2 populations (P1
and P2) with 86 and 106 plants each, respectively (derived from different BC1F1 plants) were
used. The BC1F2 plants from each population were harvested individually and planted as
BC1F3 progeny rows. The backcross derived material was screened for stripe rust resistance. A
schematic representation of population development is given in S1 Fig.
Field inoculation & resistance phenotyping
Plant material was inoculated with the mixture of major stripe rust pathotypes Pst 78S84, Pst
46S119, 110S119 and 238S119 [17]. Primary inoculations and disease pressure were built up as
per the standard protocol [12]. Infector rows of the susceptible cultivars ‘PBW 343’ and ‘HD
2967’ were planted at the borders of each population to ensure disease pressure.
The severity of stripe rust infection was recorded on individual BC1F1, BC1F2 plants and
BC1F3plantsusing a modified Cobb’s scale [22]. Disease progress was recorded at three time
points with the first observation two weeks after inoculation and second at three weeks post-
inoculation. Final disease severity was recorded when susceptible parents recorded the highest
disease severity (80S or above). For genetic analysis, the BC1F2 plants were categorized in two
classes based on individual disease reaction score. Plants with disease severity score of Ts to 5S
were considered as resistant based upon the score of resistant donor ‘Acienda’ and plants with
a score of 20S or were considered as susceptible. A Chi-squared test was used to test for good-
ness of fit with Mendelian expectations.
Genotyping
Bulked DNA of 86 BC1F3 progenies from P1 were genotyped along with the parents. Genomic
DNA from the leaves of individual plants of two weeks old seedlings of BC1F3 progenies were
extracted using the standard CTAB (Cetyl trimethyl ammonium bromide) procedure. Equal
quantity of DNA of individual plants of each BC1F3 progeny were bulked to represent BC1F2
genotype. DNA quantity was determined using a spectrophotometer and rechecked on 0.8%
agarose gels. Seven DNA samples did not pass the quality control parameters so in total 79
progenies from the population were genotyped. Approximately 200ng DNA from each sample
was used for genotyping using the Axiom1Wheat Breeders’ Array [23] which contains
35,143 SNPs using the Affymetrix GeneTitan1 system (Affymetrix Axiom1 2.0 Assay for
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PLOS ONE Novel stripe rust resistance gene from the wheat cultivar ‘Acienda’
384 samples P/N 703154 Rev. 2). The allele calling was performed using Affymetrix Analysis
Suite (version 1.1.0.616) under polyploid parameters. A Dish QC of 0.8 was used with a 90%
call rate cut-off for sample QC prior to allele calling.
The resulting SNP data was filtered by removing 5,667 SNP markers with more than 12%
missing data and 16,321 monomorphic SNP markers. In addition, 836 SNP markers giving
heterozygous calls in all samples and 9,960 markers with minor allele frequency less than 9.5
were also removed. A final set of 2,359 polymorphic SNP markers were used for further
analysis.
Statistical analysis
Chi-squared analyses were performed to determine the goodness of fit of observed segrega-
tions for stripe rust to establish the number and nature of gene(s) governing stripe rust resis-
tance. QTL mapping with Single marker analysis, Harley-Knott regression was initially carried
out using R/qtl [24] and confirmation of QTL location was performed with the ICI-mapping
software [25]. Haley-Knott method is based on multiple regression gives similar estimates as of
maximum likelihood method but it is relatively simple and computational rapid method
which makes it easier to fit models for two or more linked and/or interacting QTL. Both R/qtl
and ICIM statistical softwares are widely used as they are freely available and computationally
faster. Candidate genes in the QTL interval were identified using wheat genome RefSeq v1.0
annotation (IWGSC 2018).
Supporting information
S1 Fig. Schematic representation of plant material development.
(TIF)
S1 File.
(PDF)
Acknowledgments
The first author acknowledges the fellowship provide during her Ph.D program by Depart-
ment of Science & Technology, Govt. of India under ‘INSPIRE fellowship scheme. All authors
from PAU duly acknowledge Dr Kuldeep Singh, Director, National Bureau of Plant Genetic
Resources for procuring the European winter wheat set from NIAB, UK and sharing it with
Department of Plant Breeding and Genetics, PAU, Ludhiana.
Author Contributions
Conceptualization: Gomti Grover, Achla Sharma, Alison R. Bentley, N. S. Bains.
Data curation: Gomti Grover.
Formal analysis: Gomti Grover, Achla Sharma, Ian Mackay.
Investigation: Gomti Grover, Achla Sharma, Amanda Burridge, Sacha Przewieslik Allen,
Parveen Chhuneja.
Methodology: Gomti Grover, Satinder Kaur, Jaspal Kaur, Amanda Burridge, Parveen
Chhuneja.
Project administration: Achla Sharma, Alison R. Bentley.
Resources: Achla Sharma, Puja Srivastava, Satinder Kaur, N. S. Bains.
PLOS ONE | https://doi.org/10.1371/journal.pone.0264027 February 16, 2022 6 / 8
PLOS ONE Novel stripe rust resistance gene from the wheat cultivar ‘Acienda’
Supervision: Achla Sharma, Parveen Chhuneja.
Validation: Satinder Kaur.
Visualization: Gomti Grover, Puja Srivastava, N. S. Bains.
Writing – original draft: Gomti Grover.
Writing – review & editing: Achla Sharma, Alison R. Bentley, Parveen Chhuneja, N. S. Bains.
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