International Journal of Agriculture and Crop Sciences.

Available online at www.ijagcs.com

IJACS/2014/7-6/322-328
ISSN 2227-670X ©2014 IJACS Journal

Review: Breeding for Resistance to Soybean Rust

Faramarz sohrabi chah Hassan1*, baratali fakheri2, ali sattari3
1. Dept. of Agriculture,Payamnoor University,Tehran, Iran.
2. Associate Prof. in Plant Breeding, Dept. of Agronomy and Plant Breeding, Faculty of Agriculture, Zabol
University
3. Phd.student of Dept. of Agronomy and Plant Breeding, Faculty of Agriculture, Zabol University

Corresponding Author email: f_2000sohrabi@yahoo.com

ABSTRACT: Soybean rust (Phakopsora pachyrhizi Syd. & P. Syd.) has been a major disease limiting
soybean (Glycine max (L.) Merr.) production in the tropical and subtropical areas of Africa, Asia, and
South America, where yield losses from 10 to 80% have been reported. To successfully reduce losses
caused by pathogens, various practices such as cultural and seed sanitation techniques, fungicide
applications, and deployment of resistance are used. Fungicides are effective in managing soybean rust;
however, their application increases production costs. The development of commercial soybean cultivars
with resistance to P. pachyrhizi may be one of the most cost-effective ways to reduce yield loss. Five
dominant major soybean genes controlling resistance to ASR have been identified (Rpp1, Rpp2, Rpp3
,Rpp4 and Rpp5), these genes being located at different loci and provide resistance to different races of
P. pachyrhizi. Current studies have demonstrated that microRNAs (miRNAs) act in several plant
pathways associated with tissue proliferation, differentiation, and development and in response to abiotic
and biotic stresses.therefor information about the molecular basis of ASR–soybean interactions, which
will be needed to assist future efforts to develop effective resistance should be also considered. Molecular
markers have been successfully applied in crops for identifying the location of disease resistance loci and
for marker-assisted selection. Therefore it is obligatory to review what have already done and achieved in
the said field on soybean.
Keywords: soybean , soybean rust, marker, resistance

INTRODUCTION

The soybean crop is one of the most important crops worldwide, as the seeds are used for both protein meal and
vegetable oil. Soybean acreage covers an estimated 6% of the arable land in the world, and since the 1970s,
soybean has had the highest percent increase of hectares in production compared to any other major
crop(Hartman et al., 2011). Biotic constraints, such as pathogens, pests, and weeds, can be detrimental to
soybean production, causing significant negative impacts to yield. Pathogens and pests of soybean infect and/or
attack all parts of the plants from roots to seeds, and the extent of economic plant damage depends upon many
factors including host Susceptibility(Hartman et al., 2013) Soybean rust, caused by Phakopsora pachyrhizi, is the
most destructive foliar disease of soybean, and yield losses of over 50% are common when environmental
conditions are conducive for disease development. Heavily infected plants defoliate and mature more rapidly than
plants not infected with rust(Hartman et al., 2005). Recently, new host species from 25 genera were identified in
evaluations made in greenhouses, including 12 genera that had not been reported previously (Slaminko et al.,
2008). The rapid spread of P. pachyrhizi and the potential for severe yield losses makes this potentially the most
destructive foliar disease of soybean(Hartman et al., 2005). P. pachyrhizi is endemic in the eastern hemisphere
and has caused significant economic annual yield losses in Asia, Africa, and South America. It is believed to have
spread from Asia to Africa, then to South America, and most recently to North America(Panthee et al., 2007).
Resistance in soybean to Phakopsora pachyrhizi, the cause of soybean rust, is characterized by either reddish-
brown (RB) lesions or an immune response. The RB type of resistance can be incomplete, as evidenced by the
presence of sporulating uredinia within lesions. Susceptibility, on the other hand, is exemplified by tan-colored
(TAN) lesions, and can be expressed in gradations of susceptibility or partial resistance that are less well
defined(Miles et al., 2011). The soybean genome sequence was assembled and made available in late 2008. Since
then, The genome sequence has been used to identify the genetic basis for numerous traits, including disease
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resistance, nutritional characteristics, and developmental features. The genome sequence has provided a scaffold
for placement of many genomic feature elements, both from within soybean and from related species(Steven et al.,
2012). Microarray analysis is a useful technology for assaying transcriptional responses for biotic and abiotic plant
stresses (Bohnert et al., 2001; Moy et al., 2004). Within the first 12 h after inoculation (hai),which corresponds to
fungal germination and penetration of the epidermal cells,differential gene expression changes were evident in both
genotypes(DeMortel et al., 2007a). Cruz et al., (2013) concluded that The ASR severity was significantly reduced
on plants sprayed with ASM( Acibenzolar-S-Methyl) or supplied with Si in comparison to plants sprayed with
JA(jasmonic acid) or deionized water. breeding for resistance to soybean rust requires a thorough knowledge of the
origin, domestication, and evolution of the crop and its relatives, other major production problems, germplasm
screening methods, sources of resistant germplasm , genetics of resistance, breeding strategies and methods, and
a collaborative team of dedicated researchers with necessary resources over a long period of time(Singh et al.,
2011). Soybean crop can be successfully protected with a combination of measures ,among which the
development and utilization of resistant cultivars is most efficient,economical and ecologically most
acceptable(Vishnyakova et al., 2013). We will review the sources of resistance germplasm and recent progress
made in genetics and breeding of soybean for resistance to soybean rust. We also will briefly describe an
integrated strategy for simultaneous genetic improvement of rust resistance for cultivar development.

Pathogen – Host Interaction

Soybean rust is caused by two species, P. pachyrhizi and, less commonly, P. meibomiae (Arthur) Arthur. The
latter species (P. meibomiae), commonly known as the cause of Latin American rust or Legume rust, is found in the
western hemisphere and is not known to cause severe yield losses(Antony, 2009). The three plant responses that
have been shown to be associated with single dominant genes for soybean rust resistance are (i) an immune
response (IR); (ii) reddish-brown (RB) lesions, or incomplete resistance; and (iii) the susceptible tan (TAN) lesions
(Bromfield, 1984). The IR has only been reported with Rpp1, and only when inoculated with specific isolates
(Bonde et al., 2006; Paul and Pham, 2009). For both the RB and TAN lesion types, sporulation of uredinia has
been reported to vary (Bonde et al., 2006), although the genetics of inheritance of this trait have not been
described. For the RB reaction type, three subclasses ranging from less to more sporulation have been identified
and, for the TAN reaction type, two subclasses characterized by “few” or “many” uredinia per lesion have been
identified (Bromfield, 1984). In greenhouse inoculation studies, host–pathogen combinations that resulted in RB
lesions tended to exhibit longer latent periods and fewer and smaller uredinia than interactions producing
susceptible TAN lesions (Bonde et al., 2006; Bromfield, 1984; Marchetti, 1975). It also was shown that RB lesions
had variable color from light to dark brown, and often were larger than TAN lesions (Bonde et al., 2006). These
observations suggest that lesion color by itself is not a reliable means to rate resistance or susceptibility. The
complexity of the plant response to biotic and abiotic stresses involves many genes and biochemical and molecular
mechanisms, and adaptation to these stresses is achieved through regulating gene expression at the
transcriptional and post-transcriptional levels(Kulcheski et al., 2011).The expression profiles of differentially
expressed genes (ASR-infected compared with the mockinoculated control) revealed a biphasic response to ASR
in each genotype(DeMortel et al., 2007a). Panthee et al., (2007) conducted a cDNA microarray experiment in
soybeans in response to Asian soybean rust. The major differentially expressed gene categories were those
encoding a SA-related protein, heat shock proteins (HSP), a leaf senescence- associated receptor-like protein
kinase (LSRK), a glutathione S-transferase (GST), and chalcone isomerase (CI), which play roles in general
defense and stress tolerance. Isoflavone synthesis is associated with responses of plants to disease. In soybean
seed in particular, isoflavone accumulation is development -dependent (Dhaubhadel et al., 2007). Induction of
isoflavone- related genes at different growth stages indicates that disease response of the host plant might also
vary among growth stages. Therefore, evaluation of gene expression in response to P. pachyrhizi at various growth
stages could be helpful to identify candidate resistance genes(Panthee et al., 2009). DeMortel et al., (2007a)
concluded that timely expression of resistance genes could prevent ASR development, indicating that growth
stage-dependent gene expression is an important factor for a resistant genotype. Panthee.et al., (2009) studied the
gene expression pattern in soybean at V4 and R1 growth stage in response to P. pachyrhizi infection and found a
distinct difference between these two growth stages.

Classification Of The Resistance

Specific resistance to P. pachyrhizi is known, and seven dominant genes controlling pathotype-specific
resistance to soybean rust have been identified at five loci (Bromfield et al., 1980; Calvo et al., 2008; Chakraborty
et al., 2009). These known genes conferred resistance to some P. pachyrhizi isolates but were ineffective when
challenged with other isolates (Paul and Pham, 2009). Incompatible interactions mediated by Rpp1 have an

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immune phenotype (Miles et al., 2006), whereas resistances conferred by the other three R genes are
characterized by limited fungal growth and sporulation and the formation of reddish-brown lesions (Bonde et al.,
2006). Compatible interactions typically are characterized by tan-colored lesions with fully sporulating uredinia
(Bromfield, 1984; Bromfield and Hartwig, 1980; Miles et al., 2006). Partial or rate-reducing resistance to soybean
rust has been documented in soybean, but it has not been widely employed because of complexities in
assessment.The difficulties associated with identifying partial resistance and the ineffectiveness of specific
resistance genes has led to the suggested use of tolerance as a breeding remedy for soybean rust. Tolerance
implies susceptibility, and can be defined as the relative ability of a genotype to yield under stress from rust(Antony,
2009). Large number of genes in stress, defense and secondary metabolite category indicates that there may not
be a single mechanism to defend soybean against P. pachyrhizi infection in soybean( Panthee et al., 2009). The
race-specific resistance phenotype of Rpp2 is manifested in massive gene expression changes after the initial
response prior to the onset of rapid fungal growth that occurs in the susceptible genotype(DeMortel et al.,
2007a).Martins and Juliatti, (2012) verify the adaptability and phenotypic stability of soybean inbred lines of semi
early cycle, using rust severity as the selection trait for partial resistance and found that the strains which were the
most resistant to rust, in general, also showed the best adaptability and stability. Ribeiro et al., (2009) concluded
that Additive effects predominated in the genetic control of soybean resistance to Asian rust, and the interaction of
the segregant populations with the environment, although significant, did not alter the genetic parameter’s general
combining ability (GCA) and specific combining ability estimates, indicating that estimates obtained in one year and
one assessment can be extrapolated to others. The identification of differentially expressed plant miRNAs provides
molecular evidence for the possible involvement of miRNAs in the process of water deficit- and rust-stress
responses(Kulcheski et al., 2011). Genes related to isoflavone, carotenoid, glucosinolates, terpene biosynthesis
are of general nature related to secondary metabolites and plant defense, whereas ABC transporter, P450, GST
genes are related to disease resistance and detoxification processes( Halkier et al., 2006; Rea, 2007).

Sources Of Disease Resistance

Vavilov Institute houses the greatest in Europe collection of soybean genetic resources about 7000
accessions.For ninety years it has been the source for national breeding(Vishnyakova et al., 2013). Identification of
resistance genes is the first step toward the development of resistant varieties and gauging endogenous up-
regulation of genes in response to disease-causing agents might give indications that there could be relevant
defense genes (Panthee et al., 2009). The specific resistance gene in PI 200492 was given the designation Rpp1,
and since then four other independent dominant genes have been named: Rpp2; Rpp3; Rpp4,Rpp5 (Bromfield and
Hartwig, 1980; Mclean and Byth, 1980; Hartwig and Bromfield, 1983; Hartwig, 1986; Garcia et al., 2008) These
were tested for allelism to Rpp2 and Rpp4, and of the 26 sources reported, 23 were found to be at different loci to
Rpp2 and Rpp4. One of these sources of resistance was conditioned by a single recessive gene from the variety
Abura, and this has been incorporated in a variety (BR01-18437) destined for release in Brazil during 2008(Neto et
al., 2007). Martins & Juliatti, (2012) concluded that the lines that showed higher partial resistance to rust were UFU
001 ((Liderança x UFV 16) x (UFU18 x Br 95015308)), 006 (Canário x Conquista), 007(RC1 PI 416937 x IAC 8.2),
009 (RC2 (IAC 100 x Emgopa 302)) and 0013 ((FT 45.302 x Liderança) x (FT 4.2988 x Conquista)). In order to
identify new sources of resistance in soybean, Miles et al., (2006) evaluated the entire germplasm collection
(16,000 accessions) of the United States Department of Agriculture (USDA) against a mixture of five P. pachyrhizi
isolates. After two rounds of evaluation, only 850 accessions were identified with partial tolerance or resistance
reactions to P. pachyrhizi, which correlates to less than 5 % of USDA germplasm collection. Although specific P.
pachyrhizi strains are virulent on these single gene resistant sources, it may be beneficial to pyramid these four
known resistant genes into modern cultivars to create broad spectrum resistance to SBR in the USA.(Hartman et
al., 2005; Pierozzi et al., 2008) concluded that All commercial cultivars(BRS 184, BRS 231, BRS 232, BRSGO
Chapadões, DM 339 and Embrapa 48) showed TAN lesions, expressing susceptibility to ASR. The BR01-18437
breeding line and the plant introductions (PI 200487, PI 230970, PI 459025-A and PI 200526) expressed the RB
lesion type and were defined as carriers of major resistance genes. Ribeiro et al., (2009) concluded that BR01-
18437 line confirmed its resistance in all the environments and can be used in breeding programs for resistance to
Phakopsora pachyrhizi.The taxonomic position of soybean in the Phaseoleae tribe of the legumes means that there
are approximately two dozen other beans and relatives that have undergone independent domestication, and
which may have traits that will be useful for transfer to soybean (Steven et al., 2012). a transcriptome profiling of P.
pachyrhizi-exposed young soybean plants (V2 growth stage) using whole genome Affymetrix microarrays of
soybean indicated that A total of 112 genes were found to be differentially expressed from P. pachyrhizi exposure,
of which 46 were upregulated, and 66 were downregulated. Most of the differentially expressed genes were
general defense and stress-related genes, and 34 of these were unknown (Panthee et al., 2007).

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STRATEGY AND SELECTION METHODS

Principal factors determining strategies and methods used for breeding for resistance to soybean rust and other
desirable traits include (1) the genetic distance between the cultivar to be improved and resistant donor
germplasm, (2) the direct and indirect screening methods available, (3) the genetics of resistance, and (4) the
number of resistances and other traits to be improved(Singh et al., 2011). Various selection methods are used for
identification of those progenies which possess the most useful combinations of the desired traits .The choice of
the selection method depends on breeding objective as well as on other important factors such as the available
variability ,availability of agricultural machines and greenhouse ,size and skill of breeding team, etc(Vishnyakova et
al., 2013).The presence of multiple virulence genes in the pathogen population and the lack of multiple resistance
genes in the host provides the soybean rust pathogen with a competitive advantage. The deployment of specific
single genes for resistance is thus unlikely to be a successful strategy(Antony, 2009). Some soybean genotypes
initially identified as resistant to ASR have had this resistance broken, as has occurred with the genotypes carrying
Rpp1 and Rpp3 when exposed to the P. pachyrhizi Taiwan-72-1 isolate (Hartwig, 1986) and to the new P.
pachyrhizi isolate from the Brazilian state of Mato Grosso (MT, the Brazilian government abbreviation for this
state), the P. pachyrhizi MT state isolate, described by Yorinori et al., (2004). Soybean resistance provided by
Rpp1 and Rpp3 was defeated by the P. pachyrhizi MT isolate just two years after ASR was first detected in
Brazil(Pierozzi et al., 2008). Therefore, it is expected that breeding for polygenetic resistance may be more
effective for obtaining durable resistance or tolerance( Ribeiro et al., 2009). Maria et al., (2013) concluded that the
Asian soybean rust (ASR) symptoms can be mild on plants sprayed with Acibenzolar-S-Methyl (ASM) or supplied
with calcium silicate( a source of soluble silicon, Si) and that this amelioration likely involved the defense enzymes.
The techniques used for resistance evaluations are selected based on reliability of the results and availability of
resources (i.e., time, labor, greenhouse space, and expertise)( Hartman et al., 2013) Marker assisted selection
(MAS) strategies known as forward selection have been used effectively in soybean since the mid 1990s to pre-
screen breeding populations for simply-inherited traits(Vishnyakova et al., 2013). But many complex traits have not
been amenable to forward selection because quantitative trait loci (QTL) detected within one genetic context have
not been sufficiently predictive of other genetic contexts (Bernardo, 2008). This has prompted us to investigate a
Context Specific MAS (CSM) approach for complex traits (Sebastian et al., 2010). Soybean currently has an SSR
map that contains 1019 SSR markers distributed across 20 linkage groups (Song et al., 2004). These markers can
be used to identify the genome location of SBR resistant genes and to help quickly integrate these genes into
modern breeding lines through marker-assisted selection. Chakravarthi et al., (2006) reported the fundamental
advantages of MAS compared to conventional phenotypic selection which are:(i) Simpler compared to phenotypic
breeding (ii) Selection may be carried out at breeding stage and single plants may be selected with high reliability.
Microarray analysis is a useful technology for assaying transcriptional responses for biotic and abiotic plant
stresses (Mentewab et al., 2005; Moy et al., 2004).This technology has been used for such studies including
soybean rust caused by Phakopsora pachyrhizi (Panthee et al., 2007).

Molecular Markers
The soybean genome sequence has provided a common reference frame for genomic features (genes,
regulatory elements, transposons, other repeat sequences, markers, etc.) from both soybean and from related
species (Steven et al., 2012). DNA-based molecular markers have acted as versatile tools and have found their
own position in various fields like taxonomy, plant breeding, genetic engineering e.t.c (Joshi et al., 2011). By using
dense genetic marker maps, the contributions of separate regions of the genome on the trait values can be
estimated once the mapping population is sufficiently large. In addition, agronomic important traits like nutritional
quality, yield, flower time and durable resistance which appear to follow complex, polygenic inheritance patterns
with multiple genes having small effects on the trait value can easily by analyzed using markers. Marker Assisted
Selection (MAS) refer to the use of DNA markers that are tight-linked to target loci as a substitute for or to assist
phenotype screening. By determining the allele of a DNA marker, plants that possess particular genes or
quantitative trait loci (QTL) may be identified based on their genotype rather than their phenotype (Jonah et al.,
2011) MAS is in contrast to genetic engineering which involves the artificial insertion of such individuals genes from
one organism into the genetic material of another (typically, but not exclusively from other unrelated species
(Daniel et al., 2006). Simple sequence repeat (SSR) markers, one common marker used in marker-assisted
selection, are polymerase chain reaction (PCR)-based, are often highly polymorphic, and can be assayed on
inexpensive gel electrophoresis systems. Hyten et al., (2007) found that the Rpp1 gene is located between
Sct_187 and Sat_064 at a distance of 0.4 cM from each.

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Biotechnology
Diversity based on phenotypic and morphological characters, usually varies with environments and evaluation of
traits requires growing the plants to full maturity prior to identification, but now the rapid development of
biotechnology allows easy analysis of large number of loci distributed throughout the genome of the plants (Jonah
et al., 2011) The development of sequencing techniques and gene expression analysis on a large scale, combined
with new bioinformatics tools for data analysis have facilitated the structuring of extremely valuable databases to
create strategies for genetic engineering (Morales et al., 2012).The availability of the soybean genome sequence
has quickly enabled the identification of genes for numerous important traits(Steven et al., 2012). Microarray
analysis has been performed to aid the development of resistant varieties by identifying resistance genes
(DeMortel et al., 2007a). Transcriptional changes play a major role in plant defense process. The coordinative
upregulation genes lead to defense responses such as toxin production, cell wall structure changes, programmed
cell death, and so on. It is, therefore, important to study differentially expressed genes of soybean in response to P.
pachyrhizi, which should help to understand the mechanisms of rust development and aid towards the
development of resistant soybean varieties for Asian soybean rust (Panthee et al., 2007). Panthee et al., (2007)
found 112 genes with differential expression pattern in response to Asian soybean rust (ASR) caused by P.
pachyrhiziin soybean. those genes were not specific to the ASR rather were involved in general defense. Global
gene expression analysis has emerged as an important tool to understand how plants respond to biotic and abiotic
stresses in order to identify genes associated with specific traits (Panthee et al., 2009). Using laser capture
microdissection, Tremblay et al., (2010) isolated susceptible soybean palisade and mesophyll cells showing signs
of infection, extracted the RNA and performed transcriptome profiling. A total of 2,982 genes were differentially
expressed, from which 685 were up-regulated and 2,297 were down regulated. Complementary to transcriptional
analyses in the host, gene transcript profiling has also been performed with the fungus (Posada and Frederick,
2005; Tremblay et al., 2009). Recently, a cDNA library was constructed based on the separation of uredinia from
host tissue by using lasercaptured microdissection (Tremblay et al., 2009). About 80 % of identified genes in this
study shared no homology to previously described Phakopsora genes. This result demonstrates stage-specific
gene expression in the development of uredinia. Small, non-coding RNAs have been characterized in plants as
important factors involved in gene expression regulation in developmental processes (Mallory et al., 2006; Chen,
2005), as well as adaption to biotic and abiotic stress conditions(Lu et al., 2008; Shukla et al., 2008). Kulcheski et
al., (2011) found that Among the 11 miRNAs analyzed, all showed different expression profiles during biotic and
abiotic stresses to soybean. The pattern of miRNAs expression was different for the distinct genotypes submitted to
the pathogen stress. Most miRNAs were down regulated during the fungus infection in the susceptible genotype;
however, in the resistant genotype, most miRNAs did not vary during rust attack (Kulcheski et al., 2011).

CONCLUSIONS

Development and use of cultivars resistant to soybean rust minimize yield losses, broaden adaptation and
improve stability of performance of cultivars, reduce fungicide use and enhance fungicide use efficiency, minimize
health hazards and adverse environmental impacts and reduce production costs. Resistant varieties with genes of
greater resistance were released; however, the resistance stability is uncertain, once the large number of races of
this fungus already described proves the great variability of the pathogen. Understanding the molecular
mechanisms involved in defense responses is of primary importance for planning strategies to control stress and,
consequently, to increase plant adaptation to limiting conditions. Molecular markers have been look upon as a tools
for a large number of applications ranging from localization of a gene to improvement of plant varieties by marker-
assisted selection, called genome analysis which has generated a vast amount of information and a number of
databases are being generated to preserve and popularize it (Joshi et al., 2011). results indicated that PI 200487
and PI 200526 carry different dominant resistance major genes which are both different from Rpp2 and Rpp4. The
results also suggest that genetic resistance to ASR in the BR01-18437 breeding line is controlled by a single
recessive major gene, different from Rpp1 through Rpp4 and different from the genes of PI 200487 and PI 200526
(Pierozzil et al., 2008). Hyten et al., (2007) concluded that The tight linkage of the fl anking markers Sct_187 and
Sat_064 to Rpp1 makes these SSR markers useful for marker-assisted selection.

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