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Single Nucleotide Polymorphism Diversity and Hybridity Testing of Peanut F1 Progenies Derived from Parents with Varying Oleic Acid Content and Late Leaf Spot Resistance using SNP Markers

Guguloth Nehru1,2, Kommineni Radhika3,*
1International Crops Research Institute for the Semi-arid Tropics, Hyderabad-502 324, Telangana, India.
2Agricultural College, Bapatla, Acharya N.G. Ranga Agricultural University, Guntur-522 034, Andhra Pradesh, India.
3Director (Seeds), Acharya N.G. Ranga Agricultural University, Guntur-522 034, Andhra Pradesh, India.

  • Submitted09-01-2025|

  • Accepted14-04-2025|

  • First Online 31-05-2025|

  • doi 10.18805/LR-5469

ABSTRACT

Background: Hybridity confirmation of F1S is the key to success in any crop breeding programme. Single nucleotide polymorphism (SNP) genotyping is emerging as a fast and cost-effective tool in crop breeding programs that evaluates large segregating populations to select plants with a combination of desirable traits. SNP markers, with their high specificity and polymorphism, enable precise hybridity verification in F1 progenies.

Methods: The leaf samples were collected from parents viz., Kadiri Lepakshi, Kadiri 9 (K 9), Narayani and ICGV 201009 and F1 plants. Polymorphic SNP markers linked to oleic acid content and LLS resistance were used for genotyping. Hybridity was confirmed by analyzing heterozygosity in F1 progenies at the target loci using high-throughput genotyping platforms.

Result: Fourteen out of twenty-four SNPs were informative and polymorphic between the parents. These markers differentiated the heterozygotes (F1s) from the homozygotes efficiently. Out of 142 F1 plants, 126 plants were confirmed as hybrids using 14 highly informative SNP markers. SNP markers, snpAH00110 and snpAH00113, common in all the three crosses for the identification of hybridity, were highly polymorphic among the parents and F1S. SNP markers were very much useful for the identification of true hybrid seedlings in the early stage of growth and genotyping of the progenies more accurately for gene mapping and accelerating the breeding.

INTRODUCTION

Groundnut (Arachis hypogaea L.), also known as peanut, earthnut, monkey nut, poor man’s cashew nut, manila nut and king of oil seeds (Boraiah et al., 2012; Ravi et al., 2024; Natarajan et al., 2024) is an important oilseed, food and cash crop of Africa and Asia. Asia is the global leader with a share of 50% and 60% of the world’s groundnut area and production, respectively. In India, more than half of total groundnut production goes for oil, therefore the quantity and quality of the oil is of utmost interest to plant breeders (Sarvamangala et al., 2011; Kamalasundari et al., 2025). It is a prominent oil seed crop in India sharing about 40% of total oil production (Sunitha  et al., 2023). The quality of the oil depends on the proportion of fatty acids present in the oil. Groundnut oil contains 75-80 per cent of oleic (monounsaturated fatty acid) and linoleic acids (Polyunsaturated fatty acid), followed by 10 per cent palmitic acid and the remaining 20 per cent are stearic, arachidic, eicosenoic, behenic and lignoseric acids (Sarvamangala et al., 2011; Norden et al., 1987; Pramanik et al., 2022). Saturated fatty acids like palmitic acid have putative detrimental health effects (Carta et al., 2017). Though linoleic acid has health benefits and is an essential fatty acid in human diet; very high concentration of this fatty acid is undesirable for cooking purpose owing to its bad flavor and short shelf life due to oxidation properties (Who and Consultation, 2003). From health point of view, monounsaturated fatty acids (oleic acid) have been reported to play a vital role in reducing the risk of cardiovascular diseases by lowering the cholesterol in the blood (Kratz et al., 2002). The groundnut oil with a high oleic/linoleic acid (O/L) ratio is considered more stable oil due to its increased shelf life (Dwivedi et al., 1996).
       
Fungal diseases like leaf spots, rust, root rot, stem rot, pod rot and blight causes severe pod yield penalty and quality loss of both pods and fodder. Among the foliar fungal diseases, rust caused by Puccinia arachidis Speg., early leaf spot by Cercospora arachidicola [Hori.] and Late Leaf Spot (LLS) by Phaeoisariopsis personata [(Berk. and Curt) Deighton] are widely distributed, most destructive and economically important in India. LLS and rust can cause 50-70% pod yield loss (Subrahmanyam et al., 1984 and Janila et al., 2016) under favourable conditions. Host-resistance to LLS and rust have been reported in cultivated and wild species of Arachis spp. (Subrahmanyam et al., 1983; Pande and Rao, 2001; Sudini et al., 2015).
       
SNP markers were proven to be very powerful in the genetic analysis of other species and useful in breeding programs. SNP genotyping is emerging as a fast and cost-effective tool in crop breeding programs that evaluates large segregating populations to select plants with a combination of desirable traits. Perhaps most importantly, SNPs can be used in parallel assays and the cost per data point is favorable compared to other marker types when used in large-scale assays (Bertioli et al., 2014). This accelerated the identification of breeding lines and development of cultivars resistant to LLS, rust, root-knot nematode, stem rot, along with high oil content, high O/L content, large kernel size and tolerance to drought (Khedikar et al., 2009; Shou et al., 2010; Ravi et al., 2011; Gautami et al., 2011; Varshney et al., 2009; Pandey et al., 2017; Shasidhar et al., 2020).
               
This study was undertaken for the introgression of oleic acid content and late leaf spot resistance in to the popular cultivars Kadiri 9, Kadiri lepakshi and Narayani, well known to farmers for their high yield released from Agricultural Research Stations, Kadiri and Tirupathi, Acharya N. G. Ranga Agricultural University (ANGRAU) of Andhra Pradesh and to identify true F1S and select informative SNP markers that would help to differentiate homozygous parents and their heterogygous F1 hybrids for high oleic acid and late leaf spot resistance in peanut.

MATERIALS AND METHODS

Plant material
 
In the present study, Kadiri Lepakshi, Kadiri 9 (K 9) and Narayani, are well-known, high yielding and stable groundnut cultivars, were used as recipient parents.  Kadiri Lepakshi and Kadiri 9 (K 9) were developed at Agricultural Research Station Kadiri and released in 2002 and 2020, respectively and Narayani was developed at Regional Agricultural Research Station, Tirupathi and released in the year 2002 by Acharya N.G. Ranga Agricultural University (ANGRAU) of Andhra Pradesh. ICGV 201009 an elite Valencia and advanced breeding line of groundnut having high oleic acid content and resistance to late leaf spot, which was developed at International Crop Research Institute for the Semi-Arid Tropics, Hyderabad (ICRISAT) was used a as donor parent, (Table 1). A 24-SNP panel containing SNPs for five target traits viz., high oleic acid content, late leaf spot, fresh seed dormancy, rust and quality control were used for genotyping to confirm the presence of desirable alleles (genotype level) (Table 2).

Table 1: Characteristics of the four groundnut varieties/lines used as parents.



Table 2: List of SNPs used in ‘Fluidigm SNP Genotyping’ assays.


 
Emasculation and pollination
 
Emasculation of groundnut can be accomplished on warm bright days between afternoon and evening. The emasculated flower bud was pollinated the following morning. At ICRISAT, generally the success rate for crossing was 70 to 80% and this may vary depending on the skill of the person involved and environmental conditions, temperature and humidity in particular. Fig 1A  illustrates the steps followed in emasculation and pollination. Three independent crosses were made with Kadiri 9, Kadiri Lepakshi and Narayani serving as the pistillate parents and ICGV 201009 as the donor parent to generate F1S during rainy season 2022 in the hybridization block at ICRISAT, Patancheru, Hyderabad as described by (Nigam et al., 1990) (Table 1). A total of 142 kernels obtained from the crosses were sown in the next season to identify F1 hybrids (Table 3) in the hybridization block.

Fig 1: A) Step wise procedure for emasculation and pollination in groundnut B) Leaf tissue sampling for DNA analysis.



Table 3: Details of hybridization made during the rainy season 2022 in the hybridization block at ICRISAT, Patancheru.


 
Leaf tissue sampling for DNA analysis
 
F1 seeds from each of the three crosses were planted in the hybridization block in the bays. After 25 days of planting, a young tetra foliate leaf from each F1 plant was sampled for DNA analysis. The F1 plants to be sampled were labeled and a single hole-puncher (6.0 mm diameter) was used to punch and collect two leaf discs per sample from young and healthy newly developed tetra foliate leaf. The forceps were cleaned before and after placing each sample in a well to avoid cross contamination. The 96-well sample plates were sealed with sealing mats (AB0674, Thermo Fisher Scientific), wrapped in plastic bags, secured firmly and shipped for DNA isolation (Fig 1B).
 
Genomic DNA extraction
 
Young leaves were collected from the F1 plants and parental lines for DNA isolation. DNA was extracted using the CTAB method with minor modifications (Li et al., 2010). DNA concentration was determined using a nucleic acid detector and diluted to 20 ng μL-1 for polymerase chain reaction (PCR). SNPs were analyzed using the Fluidigm SNP Genotyping Analysis software to obtain genotype calls (Wang et al., 2009).
 
Statistical analysis
 
Data quality and estimates of genetic parameters
 
Genotyping data was converted into a HapMap file format and subjected to Quality Control (QC) analysis in TASSEL 5 (Bradbury et al., 2007) by filtering for missingness and minor allele frequency (MnAF). Summary statistics for extent of missing data, overall heterozygosity and average MnAF for the filtered data were generated using the “Geno Summary” function of the data panel in TASSEL 5. Overall, average Polymorphism Information Content (PIC) for markers using data on both F1 and their parents was estimated from the allele frequencies according to (Anderson et al., 1993) as:

where;
i = The ith allele of the jth marker.
n = The number of alleles at the jth marker.
p = Allele frequency.

Hybridity assessment
 
Initially, a general comparison was made between the F1S and the parents based on the proportion of heterozygosity obtained from TASSEL 5. Determination of the hybrid status of all F1S were based on the number of polymorphic loci that were heterozygous. Therefore, for each F1 sample, counts of SNPs detecting it as a true hybrid (heterozygous) were made and expressed as a ratio of the total number of markers that were polymorphic between its parents. Hybridity status of each F1 plant was computed as:
 

Where;
Lhet = Number of polymorphic SNPs detecting an F1 as heterozygous (true hybrid).
Pm = Total number of SNPs that are polymorphic between the parents of a particular F1.
 
Analysis of genetic relationships
 
Genetic relationship trees were created using Neighbor-Joining clustering method (Nei and Saitou, 1987) and visualized using Archaeopteryx tree viewer in TASSEL 5.

RESULTS AND DISCUSSION

A total of 126 F1 plants were confirmed as true hybrids with 24 SNP markers were analyzed with ‘Fluidigm SNP genotyping’ assay. Red, blue and green dots indicated XX (fluorescence of the FAM dye), XY (both FAM and HEX dyes) and YY (only HEX dye) types respectively. The SNP markers and their chromosomal position of 24 SNPs are presented in Table 2. The marker type of each SNP assay was divided into homozygote reference SNP (XX), homozygote alternative SNP (YY) and heterozygote (XY) (Fig 2).

Fig 2: Scatter plots of 24 ‘Fluidigm SNP genotyping’ assays.


 
Marker properties and efficiencies
 
To assess the accuracy of hybridity determination in the progenies, key genetic parameters such as major allele frequency, minor allele frequency, locus heterozygosity and polymorphic information content (PIC) of the SNP markers were evaluated. The results are illustrated in Fig 3.

Fig 3: Distrubution of major allele frequency (MAF), minor allele frquency (MnAF), proportion of locus heterozygosity and polymorphism information content (PIC).


 
Analysis of the genetic diversity of SNP markers for three crosses
 
The summary of the genetic diversity statistics of 9 SNPs for Kadiri 9 ×  ICGV 201009 is presented in Table 4a. The mean value of the major allele frequency was 0.649, ranging from 0.520 to 0.837. The average heterozygosity and PIC values were 0.599 and 0.327, respectively. Of the 9 polymorphic SNPs 6 SNPs exhibited the maximum PIC (0.37) and heterozygosity (0.837) value. The SNPs with low PIC value in the present study will not be considered for future studies on genetic diversity. The maximum heterozygosity (0.837) was observed with SNP snpAH0026, snpAH00130, snpAH00113, snpAH00135 while the minimum heterozygosity (0.245) was observed with SNPs marker snpAH0031, snpAH0033 and snpAH0037.

Table 4: Summary of statistics calculated for genetic diversity based on 14 informative SNP for three different crosses viz., Kadiri 9 × ICGV 201009, Kadiri Lepakshi × ICGV 201009 and Narayani × ICGV 201009, respectively.


       
Genetic diversity statistics of 8 SNPs for Kadiri Lepakshi ×  ICGV 201009 is presented in the Table 4b. The mean value of the major allele frequency was 0.500, ranging from 0.483 to 0.517. The average heterozygosity and PIC values were 0.925 and 0.378 respectively. Almost all SNPs exhibited the similar PIC and heterozygosity values with negligible difference.
       
Genetic diversity statistics of 11 SNPs for Narayani x ICGV 201009 is presented in the Table 4c. The mean value of the major allele frequency was 0.569. The average heterozygosity and PIC values were 0.831 and 0.37 respectively. All SNPs exhibited the same range of PIC and heterozygosity values. The SNPs with high PIC and heterozygosity values were considered as the informative SNPs for the genetic diversity studies.
       
Of the 24 SNP markers that were polymorphic only 14 SNPs were able discriminate the four parents and 126 F1 hybrids (Fig 4). The SNP marker, snpAH00110 showed the highest success rate of 90.3% to distinguish between the parents and hybrids, while SNP marker snpAH0038 showed the lowest success rate of 22.2%. Eight SNP markers comprising snpAH00113, snpAH0005, snpAH00116, snpAH00130, snpAH0026, snpAH00135, snpAH00108 and snpAH00137 had more than 50% success rate in hybrid identification among the parents and F1S. SNP markers snpAH00110 and snpAH00113 are found to be common for all the three crosses and these two markers can be used as informative markers for hybridity confirmation for particular traits.

Fig 4: SNP markers performance in hybrid identification.


 
Genetic relationships
 
Neighbor-joining clustering algorithm divided the F1S into four major groups (Fig 5A). A considerable diversity was shown within sub-clusters and the F1S. Group I has the highest number i.e, 48 F1S followed by group II, group III and group IV. The group III and IV again divided into sub groups. However, the parents were considered alone, the diversity among them were noticeable (Fig 5B), since the parents formed into four distinct groups and were highly divergent.

Fig 5: Relationship among the parents that were used to derive the F1S progenies.


       
SNP markers were used for germplasm identification, cultivar fingerprinting, true hybrid identification, genetic purity testing, parentage confirmation of hybrids and heterotic pattern in hybrids in the present investigation, the SNP markers that identified true hybrids from the three crosses viz., Kadiri 9 × ICGV 201009, Kadiri Lepakshi ×  ICGV 201009 and Narayani × ICGV 201009 were specific to each cross combination. For new crosses, similar kind of homologous markers need to be identified. Similar findings were reported for identifying true hybrids in peanut (Gomez et al., 2008 and Busisiwe et al., 2015).

CONCLUSION

The study was conducted to identify true F1 hybrids using SNP markers, with the goal of facilitating the development of inbred lines through marker-assisted selection (MAS) and marker-assisted backcrossing (MABC). The study revealed that SNP markers are effective in accurately distinguishing true heterozygous plants. Such markers are highly valuable for early-stage identification of true hybrid seedlings or target traits, as well as for precise genotyping of progenies in gene mapping studies.

CONFLICT OF INTEREST

All authors declared that there is no conflict of interest.

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