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  1. Ting NC, Jansen J, Nagappan J, Ishak Z, Chin CW, Tan SG, et al.
    PLoS One, 2013;8(1):e53076.
    PMID: 23382832 DOI: 10.1371/journal.pone.0053076
    Clonal reproduction of oil palm by means of tissue culture is a very inefficient process. Tissue culturability is known to be genotype dependent with some genotypes being more amenable to tissue culture than others. In this study, genetic linkage maps enriched with simple sequence repeat (SSR) markers were developed for dura (ENL48) and pisifera (ML161), the two fruit forms of oil palm, Elaeis guineensis. The SSR markers were mapped onto earlier reported parental maps based on amplified fragment length polymorphism (AFLP) and restriction fragment length polymorphism (RFLP) markers. The new linkage map of ENL48 contains 148 markers (33 AFLPs, 38 RFLPs and 77 SSRs) in 23 linkage groups (LGs), covering a total map length of 798.0 cM. The ML161 map contains 240 markers (50 AFLPs, 71 RFLPs and 119 SSRs) in 24 LGs covering a total of 1,328.1 cM. Using the improved maps, two quantitative trait loci (QTLs) associated with tissue culturability were identified each for callusing rate and embryogenesis rate. A QTL for callogenesis was identified in LGD4b of ENL48 and explained 17.5% of the phenotypic variation. For embryogenesis rate, a QTL was detected on LGP16b in ML161 and explained 20.1% of the variation. This study is the first attempt to identify QTL associated with tissue culture amenity in oil palm which is an important step towards understanding the molecular processes underlying clonal regeneration of oil palm.
  2. Ting NC, Zaki NM, Rosli R, Low ET, Ithnin M, Cheah SC, et al.
    J Genet, 2010 Aug;89(2):135-45.
    PMID: 20861564
    This study reports on the detection of additional expressed sequence tags (EST) derived simple sequence repeat (SSR) markers for the oil palm. A large collection of 19243 Elaeis guineensis ESTs were assembled to give 10258 unique sequences, of which 629 ESTs were found to contain 722 SSRs with a variety of motifs. Dinucleotide repeats formed the largest group (45.6%) consisting of 66.9% AG/CT, 21.9% AT/AT, 10.9% AC/GT and 0.3% CG/CG motifs. This was followed by trinucleotide repeats, which is the second most abundant repeat types (34.5%) consisting of AAG/CTT (23.3%), AGG/CCT (13.7%), CCG/CGG (11.2%), AAT/ATT (10.8%), AGC/GCT (10.0%), ACT/AGT (8.8%), ACG/CGT (7.6%), ACC/GGT (7.2%), AAC/GTT (3.6%) and AGT/ACT (3.6%) motifs. Primer pairs were designed for 405 unique EST-SSRs and 15 of these were used to genotype 105 E. guineensis and 30 E. oleifera accessions. Fourteen SSRs were polymorphic in at least one germplasm revealing a total of 101 alleles. The high percentage (78.0%) of alleles found to be specific for either E. guineensis or E. oleifera has increased the power for discriminating the two species. The estimates of genetic differentiation detected by EST-SSRs were compared to those reported previously. The transferability across palm taxa to two Cocos nucifera and six exotic palms is also presented. The polymerase chain reaction (PCR) products of three primer-pairs detected in E. guineensis, E. oleifera, C. nucifera and Jessinia bataua were cloned and sequenced. Sequence alignments showed mutations within the SSR site and the flanking regions. Phenetic analysis based on the sequence data revealed that C. nucifera is closer to oil palm compared to J. bataua; consistent with the taxanomic classification.
  3. Zolkafli SH, Ithnin M, Chan KL, Zainol Abidin MI, Ismail I, Ting NC, et al.
    Breed Sci, 2021 Apr;71(2):253-260.
    PMID: 34377073 DOI: 10.1270/jsbbs.19022
    Oil palm is continually being improved via controlled crossing of selected palms to ensure sustainable yields and productivity. As such, correct parental assignment is important as the presence of illegitimates will compromise the progress of improvement. In the present study, we determined the optimal number of microsatellite (SSR) markers for detection of illegitimates in selected oil palm crosses with high confidence. Determining the optimal number of markers to assign parentage will ensure that the DNA fingerprinting will be cost effective for routine use as a quality control tool in oil palm improvement programs. Here, we evaluated a wide range of crosses that included a cross derived from wild germplasm palm. The results revealed that markers with high PIC are informative and detect most of the alleles present in a cross, including those exhibited by the illegitimates. A larger number of optimum sets of markers are needed to detect all illegitimates for crosses with higher levels of genetic diversity. The optimal number of polymorphic SSR markers determined in the present study can ensure that appropriate quality control is implemented for oil palm improvement programs.
  4. Mohd Sanusi NSN, Rosli R, Chan KL, Halim MAA, Ting NC, Singh R, et al.
    Comput Biol Chem, 2023 Feb;102:107801.
    PMID: 36528019 DOI: 10.1016/j.compbiolchem.2022.107801
    A high-quality reference genome is an important resource that can help decipher the genetic basis of traits in combination with linkage or association analyses. The publicly available oil palm draft genome sequence of AVROS pisifera (EG5) accounts for 1.535 Gb of the 1.8 Gb oil palm genome. However, the assemblies are fragmented, and the earlier assembly only had 43% of the sequences placed on pseudo-chromosomes. By integrating a number of SNP and SSR-based genetic maps, a consensus map (AM_EG5.1), comprising of 828.243 Mb genomic scaffolds anchored to 16 pseudo-chromosomes, was generated. This accounted for 54% of the genome assembly, which is a significant improvement to the original assembly. The total length of N50 scaffolds anchored to the pseudo-chromosomes increased by ∼18% compared to the previous assembly. A total of 139 quantitative trait loci for agronomically important quantitative traits, sourced from literature, were successfully mapped on the new pseudo-chromosomes. The improved assembly could also be used as a reference to identify potential errors in placement of specific markers in the linkage groups of the genetic maps used to assemble the consensus map. The 3422 unique markers from five genetic maps, anchored to the pseudo-chromosomes of AM_EG5.1, are an important resource that can be used preferentially to either construct new maps or fill gaps in existing genetic maps. Synteny analysis further revealed that the AM_EG5.1 had high collinearity with the date palm genome cultivar 'Barhee BC4' and shared most of its segmental duplications. This improved chromosomal-level genome is a valuable resource for genetic research in oil palm.
  5. Ting NC, Chan PL, Buntjer J, Ordway JM, Wischmeyer C, Ooi LC, et al.
    Physiol Mol Biol Plants, 2023 Sep;29(9):1301-1318.
    PMID: 38024957 DOI: 10.1007/s12298-023-01360-2
    A refined SNP array containing 92,459 probes was developed and applied for chromosome scanning, construction of a high-density genetic linkage map and QTL analysis in a selfed Nigerian oil palm family (T128). Genotyping of the T128 mapping family generated 76,447 good quality SNPs for detailed scanning of aberration and homozygosity in the individual pseudo-chromosomes. Of them, 25,364 polymorphic SNPs were used for linkage analysis resulting in an 84.4% mapping rate. A total of 21,413 SNPs were mapped into 16 linkage groups (LGs), covering a total map length of 1364.5 cM. This genetic map is 16X denser than the previous version used to establish pseudo-chromosomes of the oil palm reference genome published in 2013. The QTLs associated with height, height increment and rachis length were identified in LGs TT05, 06, 08, 15 and 16. The present QTLs as well as those published previously were tagged to the reference genome to determine their chromosomal locations. Almost all the QTLs identified in this study were either close to or co-located with those reported in other populations. Determining the QTL position on chromosomes was also helpful in mining for the underlying candidate genes. In total, 55 putative genes and transcription factors involved in the biosynthesis, conjugation and signalling of the major phytohormones, especially for gibberellins and cell wall morphogenesis were found to be present in the identified genomic QTL regions, and their potential roles in plant dwarfism are discussed.

    SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s12298-023-01360-2.

  6. Ting NC, Jansen J, Mayes S, Massawe F, Sambanthamurthi R, Ooi LC, et al.
    BMC Genomics, 2014;15:309.
    PMID: 24767304 DOI: 10.1186/1471-2164-15-309
    Oil palm is an important perennial oil crop with an extremely long selection cycle of 10 to 12 years. As such, any tool that speeds up its genetic improvement process, such as marker-assisted breeding is invaluable. Previously, genetic linkage maps based on AFLP, RFLP and SSR markers were developed and QTLs for fatty acid composition and yield components identified. High density genetic maps of crosses of different genetic backgrounds are indispensable tools for investigating oil palm genetics. They are also useful for comparative mapping analyses to identify markers closely linked to traits of interest.
  7. Seng TY, Mohamed Saad SH, Chin CW, Ting NC, Harminder Singh RS, Qamaruz Zaman F, et al.
    PLoS One, 2011;6(11):e26593.
    PMID: 22069457 DOI: 10.1371/journal.pone.0026593
    Enroute to mapping QTLs for yield components in oil palm, we constructed the linkage map of a FELDA high yielding oil palm (Elaeis guineensis), hybrid cross. The parents of the mapping population are a Deli dura and a pisifera of Yangambi origin. The cross out-yielded the average by 8-21% in four trials all of which yielded comparably to the best current commercial planting materials. The higher yield derived from a higher fruit oil content. SSR markers in the public domain - from CIRAD and MPOB, as well as some developed in FELDA - were used for the mapping, augmented by locally-designed AFLP markers. The female parent linkage map comprised 317 marker loci and the male parent map 331 loci, both in 16 linkage groups each. The number of markers per group ranged from 8-47 in the former and 12-40 in the latter. The integrated map was 2,247.5 cM long and included 479 markers and 168 anchor points. The number of markers per linkage group was 15-57, the average being 29, and the average map density 4.7 cM. The linkage groups ranged in length from 77.5 cM to 223.7 cM, with an average of 137 cM. The map is currently being validated against a closely related population and also being expanded to include yield related QTLs.
  8. Yaakub Z, Kamaruddin K, Singh R, Mustafa S, Marjuni M, Ting NC, et al.
    BMC Plant Biol, 2020 Jul 29;20(1):356.
    PMID: 32727448 DOI: 10.1186/s12870-020-02563-5
    BACKGROUND: Molecular breeding has opened new avenues for crop improvement with the potential for faster progress. As oil palm is the major producer of vegetable oil in the world, its improvement, such as developing compact planting materials and altering its oils' fatty acid composition for wider application, is important.

    RESULTS: This study sought to identify the QTLs associated with fatty acid composition and vegetative traits for compactness in the crop. It integrated two interspecific backcross two (BC2) mapping populations to improve the genetic resolution and evaluate the consistency of the QTLs identified. A total 1963 markers (1814 SNPs and 149 SSRs) spanning a total map length of 1793 cM were integrated into a consensus map. For the first time, some QTLs associated with vegetative parameters and carotene content were identified in interspecific hybrids, apart from those associated with fatty acid composition. The analysis identified 8, 3 and 8 genomic loci significantly associated with fatty acids, carotene content and compactness, respectively.

    CONCLUSIONS: Major genomic region influencing the traits for compactness and fatty acid composition was identified in the same chromosomal region in the two populations using two methods for QTL detection. Several significant loci influencing compactness, carotene content and FAC were common to both populations, while others were specific to particular genetic backgrounds. It is hoped that the QTLs identified will be useful tools for marker-assisted selection and accelerate the identification of desirable genotypes for breeding.

  9. Ting NC, Yaakub Z, Kamaruddin K, Mayes S, Massawe F, Sambanthamurthi R, et al.
    BMC Genomics, 2016;17(1):289.
    PMID: 27079197 DOI: 10.1186/s12864-016-2607-4
    The commercial oil palm (Elaeis guineensis Jacq.) produces a mesocarp oil (commonly called 'palm oil') with approximately equal proportions of saturated and unsaturated fatty acids (FAs). An increase in unsaturated FAs content or iodine value (IV) as a measure of the degree of unsaturation would help to open up new markets for the oil. One way to manipulate the fatty acid composition (FAC) in palm oil is through introgression of favourable alleles from the American oil palm, E. oleifera, which has a more unsaturated oil.
  10. Ting NC, Sherbina K, Khoo JS, Kamaruddin K, Chan PL, Chan KL, et al.
    Sci Rep, 2020 10 01;10(1):16296.
    PMID: 33004875 DOI: 10.1038/s41598-020-73170-5
    Evaluation of transcriptome data in combination with QTL information has been applied in many crops to study the expression of genes responsible for specific phenotypes. In oil palm, the mesocarp oil extracted from E. oleifera × E. guineensis interspecific hybrids is known to have lower palmitic acid (C16:0) content compared to pure African palms. The present study demonstrates the effectiveness of transcriptome data in revealing the expression profiles of genes in the fatty acid (FA) and triacylglycerol (TAG) biosynthesis processes in interspecific hybrids. The transcriptome assembly yielded 43,920 putative genes of which a large proportion were homologous to known genes in the public databases. Most of the genes encoding key enzymes involved in the FA and TAG synthesis pathways were identified. Of these, 27, including two candidate genes located within the QTL associated with C16:0 content, showed differential expression between developmental stages, populations and/or palms with contrasting C16:0 content. Further evaluation using quantitative real-time PCR revealed that differentially expressed patterns are generally consistent with those observed in the transcriptome data. Our results also suggest that different isoforms are likely to be responsible for some of the variation observed in FA composition of interspecific hybrids.
  11. Singh R, Low ET, Ooi LC, Ong-Abdullah M, Nookiah R, Ting NC, et al.
    Nat Commun, 2014 Jun 30;5:4106.
    PMID: 24978855 DOI: 10.1038/ncomms5106
    Oil palm, a plantation crop of major economic importance in Southeast Asia, is the predominant source of edible oil worldwide. We report the identification of the virescens (VIR) gene, which controls fruit exocarp colour and is an indicator of ripeness. VIR is a R2R3-MYB transcription factor with homology to Lilium LhMYB12 and similarity to Arabidopsis production of anthocyanin pigment1 (PAP1). We identify five independent mutant alleles of VIR in over 400 accessions from sub-Saharan Africa that account for the dominant-negative virescens phenotype. Each mutation results in premature termination of the carboxy-terminal domain of VIR, resembling McClintock's C1-I allele in maize. The abundance of alleles likely reflects cultural practices, by which fruits were venerated for magical and medicinal properties. The identification of VIR will allow selection of the trait at the seed or early-nursery stage, 3-6 years before fruits are produced, greatly advancing introgression into elite breeding material.
  12. Singh R, Low ET, Ooi LC, Ong-Abdullah M, Ting NC, Nagappan J, et al.
    Nature, 2013 Aug 15;500(7462):340-4.
    PMID: 23883930 DOI: 10.1038/nature12356
    A key event in the domestication and breeding of the oil palm Elaeis guineensis was loss of the thick coconut-like shell surrounding the kernel. Modern E. guineensis has three fruit forms, dura (thick-shelled), pisifera (shell-less) and tenera (thin-shelled), a hybrid between dura and pisifera. The pisifera palm is usually female-sterile. The tenera palm yields far more oil than dura, and is the basis for commercial palm oil production in all of southeast Asia. Here we describe the mapping and identification of the SHELL gene responsible for the different fruit forms. Using homozygosity mapping by sequencing, we found two independent mutations in the DNA-binding domain of a homologue of the MADS-box gene SEEDSTICK (STK, also known as AGAMOUS-LIKE 11), which controls ovule identity and seed development in Arabidopsis. The SHELL gene is responsible for the tenera phenotype in both cultivated and wild palms from sub-Saharan Africa, and our findings provide a genetic explanation for the single gene hybrid vigour (or heterosis) attributed to SHELL, via heterodimerization. This gene mutation explains the single most important economic trait in oil palm, and has implications for the competing interests of global edible oil production, biofuels and rainforest conservation.
  13. Singh R, Low EL, Ooi LC, Ong-Abdullah M, Ting NC, Nookiah R, et al.
    New Phytol, 2020 04;226(2):426-440.
    PMID: 31863488 DOI: 10.1111/nph.16387
    Oil palm breeding involves crossing dura and pisifera palms to produce tenera progeny with greatly improved oil yield. Oil yield is controlled by variant alleles of a type II MADS-box gene, SHELL, that impact the presence and thickness of the endocarp, or shell, surrounding the fruit kernel. We identified six novel SHELL alleles in noncommercial African germplasm populations from the Malaysian Palm Oil Board. These populations provide extensive diversity to harness genetic, mechanistic and phenotypic variation associated with oil yield in a globally critical crop. We investigated phenotypes in heteroallelic combinations, as well as SHELL heterodimerization and subcellular localization by yeast two-hybrid, bimolecular fluorescence complementation and gene expression analyses. Four novel SHELL alleles were associated with fruit form phenotype. Candidate heterodimerization partners were identified, and interactions with EgSEP3 and subcellular localization were SHELL allele-specific. Our findings reveal allele-specific mechanisms by which variant SHELL alleles impact yield, as well as speculative insights into the potential role of SHELL in single-gene oil yield heterosis. Future field trials for combinability and introgression may further optimize yield and improve sustainability.
  14. Ooi LC, Low ET, Abdullah MO, Nookiah R, Ting NC, Nagappan J, et al.
    Front Plant Sci, 2016;7:771.
    PMID: 27446094 DOI: 10.3389/fpls.2016.00771
    Oil palm (Elaeis guineensis) is the most productive oil bearing crop worldwide. It has three fruit forms, namely dura (thick-shelled), pisifera (shell-less) and tenera (thin-shelled), which are controlled by the SHELL gene. The fruit forms exhibit monogenic co-dominant inheritance, where tenera is a hybrid obtained by crossing maternal dura and paternal pisifera palms. Commercial palm oil production is based on planting thin-shelled tenera palms, which typically yield 30% more oil than dura palms, while pisifera palms are female-sterile and have little to no palm oil yield. It is clear that tenera hybrids produce more oil than either parent due to single gene heterosis. The unintentional planting of dura or pisifera palms reduces overall yield and impacts land utilization that would otherwise be devoted to more productive tenera palms. Here, we identify three additional novel mutant alleles of the SHELL gene, which encode a type II MADS-box transcription factor, and determine oil yield via control of shell fruit form phenotype in a manner similar to two previously identified mutant SHELL alleles. Assays encompassing all five mutations account for all dura and pisifera palms analyzed. By assaying for these variants in 10,224 mature palms or seedlings, we report the first large scale accurate genotype-based determination of the fruit forms in independent oil palm planting sites and in the nurseries that supply them throughout Malaysia. The measured non-tenera contamination rate (10.9% overall on a weighted average basis) underscores the importance of SHELL genetic testing of seedlings prior to planting in production fields. By eliminating non-tenera contamination, comprehensive SHELL genetic testing can improve sustainability by increasing yield on existing planted lands. In addition, economic modeling demonstrates that SHELL gene testing will confer substantial annual economic gains to the oil palm industry, to Malaysian gross national income and to Malaysian government tax receipts.
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