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Review
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a b s t r a c t
Article history:
Received 31 March 2015
Received in revised form
17 July 2015
Accepted 20 July 2015
Available online xxx
Peanut is grown extensively in different parts of world, where various biotic and abiotic factors limit its
productivity and quality. The major fungal biotic constraints to peanut production include rust (Puccinia
arachidis Speg.), stem-rot (Sclerotium rolfsii), collar-rot (Aspergillus niger Van Teighem), aa-root (Aspergillus avus), and late leaf spot (Phaeoisariopsis personata Ber. and M A Curtis), while viral disease constraints are peanut bud necrosis disease (PBND) caused by peanut bud necrosis virus (PBNV) and peanut
stem necrosis disease (PSND) caused by tobacco streak virus (TSV). Since, only a few sources of resistance
are available in cultivated peanut for some diseases, which has resulted in the limited success of conventional breeding programmes on disease resistance. Moreover, even marker assisted breeding in
peanut is in the nascent stage and identication of some major quantitative trait loci (QTLs) for a few
fungal disease resitance genes has only recently been reported. Substantial efforts are underway to
develop PCR-based markers for the construction of high-density genetic linkage maps. This will enable
the breeders to effectively pyramid various biotic stress resistance genes into different agronomically
superior breeding populations, in a much shorter time. It is expected that the availability of various costeffective genomic resources (SNPs, whole genome sequencing, KASPar, GBS etc.) and more effective
mapping populations (NAM, MAGIC etc.) in the coming years will accelerate the mapping of complex
traits in peanut. This review provides an overview of the current developments and future prospects of
molecular marker development and their applications for improving biotic-stress resistance in peanut
crop.
2015 Elsevier Ltd. All rights reserved.
Keywords:
Genomics
Diseases and pests
Marker assisted selection
Linkage-mapping
Transgenics
1. Introduction
Peanuts (Arachis hypogaea L.), also known as groundnuts, are
grown in more than 120 countries with different agro-climatic
zones between latitudes 40 S and 40 N on approximately
21e24 M ha of land annually (Sarkar et al., 2014). It is cultivated
predominantly by small farms under low input conditions and
ranks third and fourth as a source of protein and edible oil,
respectively (Bhauso et al., 2014). Several biotic stresses are known
to limit peanut productivity, and their severity and extent of distribution vary with the cropping system, growing season, and region. Among biotic stresses, several diseases including rust
(Puccinia arachidis Speg.), early leaf spot (ELS, Cercospora arachidicola), late leaf spot (LLS, Phaeoisariopsis personata Ber. and M A
* Corresponding author.
E-mail address: gyan.gene@gmail.com (G.P. Mishra).
http://dx.doi.org/10.1016/j.cropro.2015.07.019
0261-2194/ 2015 Elsevier Ltd. All rights reserved.
rosette virus (GRV), its satellite RNA (sat RNA), and a groundnut
rosette assistor virus (GRAV)], Peanut Bud Necrosis Virus (PBND), A.
avus induced aatoxin contamination, bacterial wilt (Ralstonia
solanacearum), leafminer (Aproaerema modicella), Spodoptera, jassids (Empoasca kerri Pruthi), thrips (Frankliniella schultzei Trybom)
and termites (Odontotermes sp.) (Rao et al., 2002; Basu and Singh,
2004; Amin et al., 1985; Rao et al., 2014).
Since the 1960s, interspecic hybridization has received much
attention in peanuts because several wild Arachis species show a
very high level of resistance to many biotic stresses, such as rust,
ELS, LLS, and stem rot (Holbrook and Stalker, 2003; Singh et al.,
1984). However, success in transferring the resistance to cultivated peanuts has been limited mainly because of cross compatibility barriers, linkage drag, and long periods required for
developing stable tetraploid interspecic derivatives (Wynne et al.,
1991; Singh et al., 1997). Moreover, the partial and polygenic nature
of biotic stresses makes the identication of resistant and susceptible lines very tedious using conventional screening techniques
(Leal-Bertioli et al., 2009). Because of the frequent occurrence of
multiple diseases, peanut yields are often signicantly lower than
their potential (Holbrook and Stalker, 2003). In the future, cultivars
with multiple disease and pest resistances will be needed, which
appears to be a very difcult endeavour for this crop species (Basu
and Singh, 2004).
Marker-assisted selection (MAS) offers great promise for
improving the efciency of conventional plant breeding (Janila
et al., 2013), including the potential to pyramid resistance genes
in peanuts (Mishra et al., 2009; Varshney et al., 2014; Pandey et al.,
2012). For any molecular breeding program, assessment of genetic
diversity and development of genetic linkage maps are two very
important steps (Dwivedi et al., 2003). Abundant polymorphisms in
wild Arachis species have been observed, but progress in the molecular breeding of cultivated peanuts is greatly constrained due to
the low level of detectable molecular genetic variation (Mondal
et al., 2005; Herselman, 2003; Raina et al., 2001; He and Prakash,
2001). Therefore, the use of more robust assays such as single
nucleotide polymorphisms (SNPs), competitive allele-specic PCR
(KASPar) and genotyping by sequencing (GBS) approaches are
needed. However, cost-effective SNP genotyping platforms are not
readily available for tetraploid peanuts, but a large number of
robust markers such as SSRs and SNPs (including KASPar) would be
valuable. SSRs are still considered the marker of choice in peanuts
(Pandey et al., 2012), and a wide range of genotypes have been used
for mapping (Table 1) of many important biotic and abiotic traits
using SSR markers (Table 2).
Despite being an important oilseed crop, very limited work in
the area of molecular genetics and breeding of peanuts has been
performed (Dwivedi et al., 2002; Raina et al., 2001). However, over
the last decade, signicant developments have been made in the
use of various molecular approaches for biotic stress management
in peanuts, and new efforts such as functional genomics are likely
to play key roles in the future (Wang et al., 2011; Varshney et al.,
2014; Gajjar et al., 2014). Recently, Kanyika et al. (2015) has
75
Table 1
List of a few genotypes, used for mapping of various resistance gene(s) (Dwivedi et al., 2003; Shoba et al., 2012;
Sujay et al., 2012).
Traits
Genotypes
76
Table 2
SSR markers and its linkage group known to be associated to the rust and/or LLS resistance gene(s).
S. No.
Primers
Linkage group
Cross/genotypes
Resistance
Reference
1
2
seq3A01238a
seq5D05274
a07
b07and a07
Rust
Rust and LLS
3
4
seq16F01271
seq17F06152
b03
b04
Rust
Rust and LLS
seq13A07265
b01
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
seq2F05280
seq8E12200
seq16C06263
seq13A10250
seq2B10290
IPAHM103160
PM384100
PM137150
PM03168
PMc588183
PM375102
seq8D09190
GM1536410
GM2301137
GM2079418
PM50110
PM35124
b02
a01
b03
b04
b03
a03 and b03
e
b06
a03 and b03
e
a04
b10 and a09
b03
b03
b03
b05
a06 and b04
22 genotypes
22 genotypes
22 genotypes
22 genotypes
22 genotypes
TAG 24 xGPBD 4
TMV 2 COG 0437
TMV 2 COG 0437
TMV 2 COG 0437
TMV 2 COG 0437
TMV 2 COG 0437
TAG 24 GPBD 4
TG 26 xGPBD 4
TG 26 xGPBD 4
TG 26 xGPBD 4
20 genotypes
20 genotypes
23
seq4A05 and
gi56931710
a03
(F2)
(F2)
(F2)
(F2)
(F2)
Rust
77
78
Disease/Causal organism
Reference
RAPD
RFLP
AFLP
AFLP
AFLP
SCAR
RAPD
AS-PCRa
RAPD
AFLP and SSR
AFLP
AFLP
SSR
RAPD and ISSR
SSR
ISSR
SSR
Microarray
EST-SSR
SNP
TEa
Nematode
Nematode
Bacterial wilt
Rosette disease
A. avus
A. avus
Pod-rot
Nematode
Rust
Bacterial wilt
Rust
LLS
Sclerotinia blight
Rust and LLS
Nematode
Rust and LLS
A. avus
A. avus
Rust
Rust and Leaf spots
Rust
Table 4
List some classical and latest genetic linkage maps.
Populations
Marker(s)/Loci
References
F2
Back Cross
Arachis duranensis
02 RILs
02 RILs
10 RILs, 01 BC
03 RILs
RFLP
RFLP
1724 marker loci
324 marker loci
225 SSR
897 marker loci
3693 marker loci
1063.0
2210.0
1081.3
1352.1
1152.9
3863.6
2651.0
79
Table 5
List of QTLs identified for various biotic-stress related traits in peanut.
Traits
No of QTLs identied
Reference
LLS
28
10.07e67.8
Leaf rust
Aspergillus avus
Bruchid resistance
Aphid vector of rosette disease
In F2 map
TSWV
Leaf spot
Thrips
In F5 map
Thrips
TSWV
Leaf spot
LLS
TSWV
LLS
13
6
13
8
54 (Total)
15
37
02
23 (Total)
01
09
13
05
01
03
2.54e82.62
6.2e22.7
13e82
1.18e76.16
e
4.40e34.92
6.61e27.35
12.14e19.43
e
5.86
5.20e14.14
5.95e21.45
4.2e43.8
16.7
12.42e20.59
identified and cloned the resistance gene to TSWV and characterized two peanut oxalate oxidase genes.
In response to A. avus infection, many genes were found to be
up-regulated in peanuts, of which PR-10 and pathogenesis-induced
protein (PIP) genes were cloned (Xie et al., 2009a,b). Resveratrol
imparts resistance in plants against both UV radiation and fungal
infection; the gene that synthesizes resveratrol synthase has been
cloned from peanuts, and expression analysis indicates that it is
expressed in the root (Zhou et al., 2008; Han et al., 2010). Lipid
transfer proteins (LTP), which were reported to be involved in
disease resistance in plants, have also been cloned from peanuts
(Zhao et al., 2009).
Transcriptome analysis of the migratory plant parasitic nematode Ditylenchus africanus (peanut pod nematode) from mixed
stages revealed the involvement of putative proteins in developmental and reproductive processes, as well as the role of unigenes
in oxidative stress and anhydrobiosis (Haegeman et al., 2009). Eight
differentially expressed genes were identified in A. stenosperma
roots in response to M. arenaria infection using in silico ESTs and
~es et al., 2010, 2011).
microarray analysis (Guimara
From non-protein coding genes, microRNAs were transcribed by
RNA polymerase II (Kim, 2005), and understanding of its functional
and regulatory roles could open new windows for crop improvement including disease tolerance. Zhao et al. (2010) and Pan and Liu
(2010) have identied 89 peanut miRNAs belonging to 14 new
miRNA and 22 conserved miRNA families, which can provide the
basis for peanut miRNA research for resistance to different stresses.
Relationships between functional molecules and plant phenotypes
can be studied more specically using proteomics (Wang et al.,
2011), and proteins that may play roles in aatoxin resistance in
imbedded peanut seeds have been discovered through proteomic
studies (Wang et al., 2008b).
In eukaryotes, epigenetic regulation is known to contribute to
gene silencing and plays critical roles in development and genome
defence against viruses, transposons, and transgenes (Lister et al.,
2008; Gehring et al., 2006; La et al., 2011). It has been observed
that bacterially infected plant tissue shows a net reduction in DNA
methylation, which may affect the disease resistance genes
responsible for surveillance against pathogens (Alvarez et al., 2010).
An investigation regarding epigenetic regulation mechanisms of
the peanut allergen gene Arah3 in developing peanut embryos
demonstrated an association between the loss of histone H3 from
the proximal promoter and high expression of Arah3 during embryo maturation (Fu et al., 2010). For better understanding and
management of various biotic stresses in peanuts, there is an urgent
80
81
Table 6
Transgenics developed for various biotic stress resistances in peanut.
Genes
Resistance
Reference
Coat protein
cry1AC
Nucleocapsid (N)
Cowpea trypsin inhibitor gene
Coat protein
Chitinase and glucanase
Barley oxalate oxidase
cry1EC
cry1X
cry1EC and Chi11
Coat Protein gene PStV
Mustard defensin
Chloroperoxidase (cpo-p)
Rice chitinase-3
Rchit and CHI
SniOLP and Rs-AFP2
Rice chitinase gene (Rchit)
Coat protein
cry1AcF
cry8Ea1
Tfgd2-RsAFP2 fusion gene
PBND
Elasmopalpus lignoscellus
Tomato spotted wilt virus
Insect tolerance
Peanut stripe potyvirus
Sclerotinia blight
Sclerotinia blight
Spodoptera litura
Helicoverpa armigera and Spodoptera litura
Spodoptera litura and Phaeoisariopsis personata
PStV
LLS
A. avus
Leaf spot
Fusarium wilt and Cercospora arachidicola
LLS
A. avus, LLS and rust
PSND
Spodoptera litura
Holotrichia parallela
ELS and LLS
82
Fig. 1. An outline of tentative biotechnological interventions proposed for the development peanut genotypes resistant to various biotic-stresses.
~es, P.M.,
Alves, D.M.T., Pereira, R.W., Leal-Bertioli, S.C.M., Moretzsohn, M.C., Guimara
Bertioli, D.J., 2008. Development and use of single nucleotide polymorphism
markers for candidate resistance genes in wild peanuts (Arachis spp). Genet.
Mol. Res. 7, 631e642.
Amin, P.W., Singh, K.N., Dwivedi, S.L., Rao, V.R., 1985. Sources of resistance to the
jassid (Empoasca kerri Pruthi), thrips (Frankliniella schultzei (Trybom)) and termites (Odontotermes sp.) in groundnut (Arachis hypogaea L.). Peanut Sci. 12,
58e60.
Anuradha, S.T., Divya, K., Jami, S.K., Kirti, P.B., 2008. Transgenic tobacco and peanut
plants expressing a mustard defensin show resistance to fungal pathogens.
Plant Cell Rep. 27, 1777e1786.
Arumuganatham, E., 1991. Nuclear DNA content of some important plant species.
Plant Mol. Biol. Rep. 9, 211e215.
Azzam, C.R., Azer, S.A., Khaleifa, M.M., Abol-Ela, M.F., 2007. Characterization of
peanut mutants and molecular markers associated with resistance to pod rot
diseases and aatoxin contamination by RAPD and ISSR. Arab. J. Biotechnol. 10,
301e320.
Bala, M., Radhakrishnan, T., Kumar, A., Mishra, G.P., Dobraia, J.R., Kirti, P.B., 2015.
Overexpression of a fusion defensin genes from radish and fenugreek improves
resistance against leaf spot diseases caused by Cercospora arachidicola and
Phaeoisariopsis personata in peanut. Turk. J. Biol. http://dx.doi.org/10.3906/biy1412-46 (in press).
Barros, G.G., Chiotta, M.L., Reynoso, M.M., Torres, A.M., Chulze, S.N., 2007. Molecular
characterization of Aspergillus section Flavi isolates collected from peanut elds
in Argentina using AFLPs. J. Appl. Microbiol. 103, 900e909.
Basu, M.S., Singh, N.B., 2004. Cytogenetics and utilization of Arachis species. In:
Basu, M.S., Singh, N.B. (Eds.), Groundnut Research in India. National Research
Centre for Groundnut, Junagadh, Gujarat, India.
Beena, M.R., Tuli, R., Gupta, A.D., Kirti, P.B., 2008. Transgenic peanut (Arachis
hypogaea L.) plants expressing cry1EC and rice chitinase cDNA (Chi11) exhibit
resistance against insect pest Spodoptera litura and fungal pathogen Phaeoisariopsis personata. Trans. Plant J. 2, 157e164.
Bertioli, D.J., Leal-Bertioli, S.C.M., Lion, M.B., Santos, V.L., Pappas, G., Cannon, S.B.,
Guimaraes, P.M., 2003. A large scale analysis of resistance gene homologues in
Arachis. Mol. Genet. Genomics 270, 34e45.
Bhauso, T.D., Radhakrishnan, T., Kumar, A., Mishra, G.P., Dobaria, J.R., Rajam, M.V.,
2014. Over-expression of bacterial mtlD gene confers enhanced tolerance to
salt-stress and water-decit stress in transgenic peanut (Arachis hypogaea)
through accumulation of mannitol. Aust. J. Crop Sci. 8, 413e421.
Bosamia, T.C., Mishra, G.P., Radhakrishnan, T., Dobaria, J.R., 2015. Novel and stress
relevant EST derived SSR markers developed and validated in peanut. PLoS One
10 (6), e0129127. http://dx.doi.org/10.1371/journal.pone.0129127.
Burow, M.D., Simpson, C.E., Paterson, A.H., Starr, J.L., 1996. Identication of peanut
(Arachis hypogaea L.) RAPD markers diagnostic of root-knot nematode (Meloidogyne arenaria (Neal) Chitwood) resistance. Mol. Breed. 2, 369e379.
Burow, M.D., Simpson, C.E., Starr, J.L., Paterson, A.H., 2001. Transmission genetics of
chromatin from a synthetic amphiploid in cultivated peanut (Arachis hypogaea
L.): Broadening the gene pool of a monophyletic polyploid species. Genetics
83
84
improvement: use of genetic and genomic tools. Front. Plant Sci. 4, 23. http://
dx.doi.org/10.3389/fpls.2013.00023.
Jiang, H.F., Chen, B.G., Ren, X.P., Laio, B.S., Lei, Y., Fu, T.D., Ma, C.Z., Mace, E.,
Crouch, J.H., 2007b. Identication of SSR markers linked to bacterial wilt
resistance of peanut with RLs. Chin. J. Oil Crop Sci. 29, 26e30.
Jiang, H.F., Liao, B.S., Ren, X.P., Lei, Y., Mace, E., Fu, T.D., Crouch, J.H., 2007a.
Comparative assessment of genetic diversity of peanut (Arachis hypogaea L.)
genotypes with various levels of resistance to bacterila wilt through SSR and
AFLP analyses. J. Genet. Genomics 34, 544e554.
Jiang, H.F., Ren, X.P., Lei, Y., Liao, B.S., Mace, E., Crouch, J.H., 2003. Study on molecular
marker of peanut resistance to bacterial wilt. J. Peanut Sci. 32 (sup), 319e323.
Kamdar, J.H., Goswami, B.R., Bera, S.K., 2014. Genetic molecular diversity in interspecic peanut lines differing in temporal resistance to peanut bud necrosis
disease. Afr. J. Biotechnol. 3, 385e393.
Kanazin, V., Talbert, H., See, D., DeCamp, P., Nevo, E., Blake, T., 2002. Discovery and
assay of single-nucleotide polymorphisms in barley (Hordeum vulgare). Plant
Mol. Biol. 48, 529e537.
Kanyika, B.T.N., Lungu, D., Mweetwa, A.M., Kaimoyo, E., Njung'e, V.M., Monyo, E.S.,
Siambi, M., He, G., Prakash, C.S., Zhao, Y., deVilliers, S.M., 2015. Identification of
groundnut (Arachis hypogaea) SSR markers suitable for multiple resistance
traits QTL mapping in African germplasm. Elect. J. Biotechnol. 18, 61e67.
Kelly, D., Chamberlin, C., Melouk, H.A., Payton, M.E., 2010. Evaluation of the U.S.
peanut mini core collection using a molecular marker for resistance to Sclerotinia minor Jagger. Euphytica 172, 109e115.
Keshavareddy, G., Rohini, S., Ramu, S.V., Sundaresha, S., Kumar, A.R.V., Kumar, P.A.,
Udayakumar, M., 2013. Transgenics in groundnut (Arachis hypogaea L.)
expressing cry1AcF gene for resistance to Spodoptera litura (F.). Physiol. Mol.
Biol. Plants 19, 343e352.
Khedikar, Y.P., Gowda, M.V.C., Sarvamangala, C., Patgar, K.V., Upadhyaya, H.D.,
Varshney, R.K., 2010. A QTL study on late leaf spot and rust revealed one major
QTL for molecular breeding for rust resistance in groundnut (Arachis hypogaea
L.). Theor. Appl. Genet. 121, 971e984.
Khera, P., Upadhyaya, H.D., Pandey, M.K., Roorkiwal, M., Sriswathi, M., Janila, P.,
Guo, Y., McKain, M.R., Nagy, E.D., Knapp, S.J., Mack, J.L., Conner, J.A., Akins, P.O.,
Varshney, R.K., 2013. Single nucleotide polymorphism-based genetic diversity
in the reference set of peanut (Arachis spp.) by developing and applying costeffective kompetitive allele specic polymerase chain reaction genotyping assays. Plant Genome. http://dx.doi.org/10.3835/plantgenome2013.06.0019.
Kim, V.N., 2005. MicroRNA biogenesis: coordinated cropping and dicing. Nat. Rev.
Mol. Cell Biol. 6, 376e385.
Kolte, S.J., 1984. Peanut diseases. In: Diseases of Annual Oilseed Crops, 1. CRC Press,
Inc, pp. 30e37.
Krishna, G., Singh, B.K., Kim, E.K., Morya, V.K., Ramteke, P.W., 2015. Progress in
genetic engineering of peanut (Arachis hypogaea L.) e a review. Plant Biotechnol. J. 13, 147e162.
La, H., Ding, B., Mishra, G.P., Zhou, B., Yang, H., Bellizzi, M.D.R., Chen, S., Meyers, B.,
Peng, Z., Zhu, J.K., Wang, G.L., 2011. A 5-methylcytosine DNA glycosylase/lyase
demethylates the retrotransposon Tos17 and promotes its transposition in rice.
Proc. Nat. Acad. Sci. U. S. A. 108, 15498e15503.
, V.F., Alves-Freitas, D.M.T., Moretzsohn, M.C.,
Leal-Bertioli, S.C.M., Carolina, A., Jose
~es, P.M., Nielen, S., Vidigal, B.S., Pereira, R.W., Pike, J., Fa
vero, A.P.,
Guimara
Parniske, M., Varshney, R.K., Bertioli, D.J., 2009. Identication of candidate
genome regions controlling disease resistance in Arachis. BMC Plant Biol. 9,
112e123. http://dx.doi.org/10.1186/1471-2229-9-112.
Lei, Y., Liao, B.S., Wang, S.Y., Li, D., Jiang, H.F., 2005. Identication of AFLP markers for
resistance to seed infection by Aspergillus avus in peanut (Arachis hypogaea L.).
Acta Agron. Sin. 31, 1349e1353.
Lei, Y., Liao, B.S., Wang, S.Y., Zhang, Y.B., Li, D., Jiang, H.F., 2006. A SCAR marker for
resistance to Aspergillus avus in peanut (Arachis hypogaea L.). Yi Chuan 28,
1107e1111.
Liang, X., Chen, X., Hong, Y., Liu, H., Zhou, G., Li, S., Guo, B., 2009. Utility of ESTderived SSR in cultivated peanut (Arachis hypogaea L.) and Arachis wild species. BMC Plant Biol. 9, 35. http://dx.doi.org/10.1186/1471-2229-9-35.
Lister, R., O'Malley, R.C., Tonti-Filippini, J., Gregory, B.D., Berry, C.C., Millar, A.H.,
Ecker, J.R., 2008. Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell 133, 523e536.
Liu, Y., Liu, Z., Hamada, M.S., Yin, Y.N., Ma, Z.H., 2014. Characterization of laboratory
pyrimethanil-resistant mutants of Aspergillus avus from groundnut in China.
Crop Prot. 60, 5e8.
Livingstone, D.M., Hampton, J.L., Phipps, P.M., Grabau, E.A., 2005. Enhancing resistance to Sclerotinia minor in peanut by expressing a barley oxalate oxidase gene.
Plant Physiol. 137, 1354e1362.
Luo, M., Dang, P., Bausher, M.G., Holbrook, C.C., Lee, R.D., Lynch, R.E., Guo, B.Z.,
2005b. Identication of transcripts involved in resistance responses to leaf spot
disease caused by Cercosporidium personatum in peanut (Arachis hypogaea).
Phytopathology 95, 381e387.
Luo, M., Liang, X.Q., Dang, P., Holbrook, C.C., Bausher, M.G., Lee, R.D., Guo, B., 2005a.
Microarray based screening of differentially expressed genes in peanut in
response to Aspergillus parasiticus infection and drought stress. Plant Sci. 169,
695e703.
Mace, E.S., Phong, D.T., Upadhyaya, H.D., Chandra, S., Crouch, J.H., 2006. SSR analysis
of cultivated groundnut (Arachis hypogaea L.) germplasm resistant to rust and
late leaf spot diseases. Euphytica 152, 317e330.
Magbanua, Z.V., Wilde, H.D., Roberts, J.K., Chowdhury, K., Abad, J., Moyer, J.W.,
Wetzstein, H.Y., Parrott, W.A., 2000. Field resistance to tomato spotted wilt virus
85
86
Yang, H., Ozias-Akins, P., Culbreath, A.K., Gorbet, D.W., Weeks, J.R., Mandal, B.,
Pappu, H.R., 2004. Field evaluation of Tomato spotted wilt virus resistance in
transgenic peanut (Arachis hypogaea). Plant Dis. 88, 259e264.
Yang, H., Singsit, C., Wang, A., Gonsalves, D., Ozias-Akins, P., 1998. Transgenic peanut
plants containing a nucleocapsid protein gene of tomato spotted wilt virus
show divergent levels of gene expression. Plant Cell Rep. 17, 693e699.
Yeri, S.B., Shirasawa, K., Pandey, M.K., Gowda, M.V.C., Sujay, V., Shriswathi, M.,
Nadaf, H.L., Motagi, B.N., Lingaraju, S., Bhat, A.R.S., Varshney, R.K.,
Krishnaraj, P.V., Bhat, R.S., 2014. Development of NILs from heterogeneous
inbred families for validating the rust resistance QTL in peanut (Arachis hypogaea L.). Plant Breed. 133, 80e85.
Yuksel, B., Estill, J.C., Schulze, S.R., Paterson, A.H., 2005. Organization and evolution
of resistance gene analogs in peanut. Mol. Genet. Genomics 274, 248e263.
Zhao, C.Z., Li, A.Q., Wang, X.J., Xia, H., Su, L., Li, C.S., 2009. Cloning and expression
analysis of lipid-transfer protein family genes in Arachis hypogaea L. J. Peanut
Sci. 4, 15e20.
Zhao, C.Z., Xia, H., Frazier, T.P., Yao, Y.Y., Bi, Y.P., Li, A.Q., Li, M.J., Li, C.S., Zhang, B.H.,
Wang, X.J., 2010. Deep sequencing identies novel and conserved microRNAs in
peanuts (Arachis hypogaea L.). BMC Plant Biol. 10, 3. http://dx.doi.org/10.1186/
1471-2229-10-3.
Zhou, Y.Q., Yang, Y.Y., Huang, J.Q., Liao, B.S., 2008. Cloning and analysis of resveratrol
synthase gene family. Chin. J. Oil Crop Sci. 30, 162e167.
Zhuang, D.H., Zou, X.H., Zhou, M., Zheng, Y.X., Zhong, Q.M., Hu, Z., Cao, J., Chen, X.Y.,
Chen, F.Q., 2003. Studies on Agrobacterium tumefaciens-mediated genetic
transformation of peanut (Arachis hypogaea L.). Chin. J. Oil Crop Sci. 25, 47e51.