Skip to main content
SpringerLink
Log in

DArTseq Molecular Markers Associated with the Spiny-Tip Leaf Margin in Pineapple (Ananas comosus L.)

Tropical Plant Biology volume 13, pages 91–116 (2020)Cite this article

Abstract

A genome-wide association study (GWAS) and quantitative trait loci (QTL) analysis using two bi-parental (parental cultivars Smooth Cayenne and MD-2) pineapple seedling populations segregating for spiny and spiny-tip leaf margin and 12 wild and pre-Columbian domesticated genotypes were used to identify single nucleotide polymorphism (SNP) and silicoDArT markers associated with the spiny-tip leaf margin phenotype in pineapple. One QTL between the nucleotide positions 14,355,639 and 14,368,806 on linkage group six (LG06) was identified using SNP markers and one QTL between the nucleotide positions 14,330,844 and 14,346,378 using silicoDArT markers. GWAS and QTL analysis methods identified the same most significantly associated SNP and silicoDArT markers. The most significantly associated SNP and silicoDArT markers were positioned at 14,355,639 and 14,341,745 bp respectively, on or very near, a zeaxanthin epoxidase (ZEP) gene, a key gene in the abscisic acid (ABA) pathway. Other associated genes with a high significance by GWAS analysis using at least two algorithms include a detoxification 33-like (DTX) and a resistance gene analog (RGA2-like). It is proposed that a polymorphism in the putative ZEP gene is the main causal variant associated with the spiny-tip leaf margin in ‘Smooth Cayenne’ pineapple and its descendants including ‘MD-2’.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

ABA:

Abscisic acid

BLAST:

Basic local alignment search tool

CLV:

Clavata

DArT:

Diversity Arrays Technology

DTX:

Detoxification

ECMLM:

Enriched compressed mixed linear model

EMMA:

Efficient mixed model association

ERf:

ERECTA family

FarmCPU:

Fixed and random model circulating probability unification

FPKM:

Fragments per kilobase of transcript per million mapped reads

FTIP:

FT-interacting protein

GA:

Gibberellic acid

GATL:

Galacturonosyltransferase-like

GAUT:

Galacturonosyltransferase

GWAS:

Genome wide association study

KNNi:

k-nearest neighbour imputation

KNOX:

KNOTTED-like homeobox

LD:

Linkage disequilibrium

LG:

Linkage group

LRR:

Leucine-rich repeat

MAF:

Minor allele frequency

MATE:

Multi-drug and toxic extrusion

MLMM:

Multi-locus mixed linear model

MT:

Microtubule

MVP:

Memory-efficient, Visualization-enhanced, and Parallel-accelerated Tool for Genome-Wide Association Study

NBS-LRR:

Nucleotide binding site – Leucine rich repeat

P3D:

Population parameters previously determined

PGD:

Pineapple Genomics Database

QQ plot:

Quantile-Quantile plot

QTL:

Quantitative trait loci

RGA:

Resistance Gene Analog

SAM:

Shoot apical meristem

SK13:

Shaggy-like kinase 13

SNP:

Single nucleotide polymorphism

SUPER:

Settlement of MLM under progressively exclusive relationship

TBCC:

Tubulin binding cofactor

TPR:

Tetratricopeptide repeat-containing

WUS:

Wuschel

ZEP:

Zeaxanthin epoxidase

References

  • Abe T, Thitamadee S, Hashimoto T (2004) Microtubule defects and cell morphogenesis in the lefty1lefty2 tubulin mutant of Arabidopsis thaliana. Plant Cell Physiol 45(2):211–220

    CAS  PubMed  Google Scholar 

  • Acquaviva C, Pines J (2006) The anaphase-promoting complex/cyclosome: APC/C. J Cell Sci 119(12):2401–2404

    CAS  PubMed  Google Scholar 

  • Ariizumi T, Lawrence PK, Steber CM (2011) The role of two F-box proteins, SLEEPY1 and SNEEZY, in Arabidopsis gibberellin signalling. Plant Physiol. https://doi.org/10.1104/pp.110.166272

    PubMed  PubMed Central  Google Scholar 

  • Barghetti A, Sjogren L, Floris M et al (2017) Heat-shock protein 40 is the key farnesylation target in meristem size control, abscisic acid signalling, and drought resistance. Genes Dev 31:2282–2295

    CAS  PubMed  PubMed Central  Google Scholar 

  • Barrero JM, Piqueras P, Gonzalez-Guzman M et al (2005) A mutational analysis of the ABA1 gene of Arabidopsis thaliana highlights the involvement of ABA in vegetative development. J Exp Bot 56(418):2071–2083

    CAS  PubMed  Google Scholar 

  • Barrett JC, Fry B, Maller J, Daly MJ (2005) Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21(2):263–265

    CAS  PubMed  Google Scholar 

  • Blancaflor EB, Hou G, Chapman KD (2003) Elevated levels of N-lauroylethanolamine, an endogenous constituent of desiccated seeds, disrupt normal root development in Arabidopsis thaliana seedling. Planta 217:206–217. https://doi.org/10.1007/s00425-003-0985-8

    Article  CAS  PubMed  Google Scholar 

  • Blancaflor EB, Kilaru A, Keereetaweep J, Khan BR, Faure L, Chapman KD (2014) N-Acylethanolamines: lipid metabolites with function in plant growth and development. Plant J 79:568–583. https://doi.org/10.1111/tpj.12427

    Article  CAS  PubMed  Google Scholar 

  • Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635

    CAS  PubMed  Google Scholar 

  • Burko Y, Geva Y, Refael-Cohen A, Shleizer-Burko S, Shani E, Berger Y, Halon E, Chuck G, Moshelion M, Ori N (2011) From organelle to organ: ZRIZI MATE-type transporter is an organelle transporter that enhances organ initiation. Plant Cell Physiol 52(3):518–527

    CAS  PubMed  Google Scholar 

  • Caffall KH, Pattathil S, Phillips SE, Hahn MG, Mohnen D (2009) Arabidopsis thaliana T-DNA mutants implicate GAUT genes in the biosynthesis of pectin and xylan in cell walls and seed testa. Mol Plant 2(5):1000–1101

    CAS  PubMed  Google Scholar 

  • Cao SQ, Ye M, Huang Q et al (2006) A role for SPINDLY gene in the regulation of oxidative stress response in Arabidopsis. Russ J Plant Physiol 53(4):541–547

    CAS  Google Scholar 

  • Cao K, Zheng Z, Wang L et al (2014) Comparative population genomics reveals the domestication history of the peach, Prunus persica, and human influences on perennial fruit crops. Genome Biol 15:415 https://genomebiology.com/2014/15/7/415Accessed 30 Dec 2019

  • Chen L-Y, VanBuren R, Paris M et al (2019) The bracteatus pineapple genome and domestication of clonally propagated crops. Nat Genet (in press) 51: 1549-1558https://doi.org/10.1038/s41588-019-0506-8

    CAS  PubMed  Google Scholar 

  • Cheng L, Ni X, Zheng M, Sun L, Wang X, Tong Z (2018) Expressional characterization of galacturonosyltransferase-like gene family in Eucalyptus grandis implies a role in abiotic stress responses. Tree Genet Genomes 14(81):1–11. https://doi.org/10.1007/s11295-018-1294-5

    Article  Google Scholar 

  • Collins JL (1960) The pineapple. Botany, cultivation and utilization. Interscience Publishers Inc, New York

    Google Scholar 

  • Coppens d’Eeckenbrugge G, Sanewski G (2011) Leaf margin in pineapple. Pineapple News 18:32–37 http://www.ishs-horticulture.org/workinggroups/pineapple/PineNews18.pdfAccessed 30 Dec 2019

  • Coppens d’Eeckenbrugge G, Duval M-F, Leal F (2018) The pineapple success story: from domestication to pantropical diffusion. In: Ming R (ed) Genetics and genomics of pineapple: crops and models 22. Springer, Cham

    Google Scholar 

  • Crowell DN, Huizinga DH (2008) Protein isoprenylation: the fat of the matter. Trends Plant Sci 14(3):163–170

    Google Scholar 

  • Cuming AC, Stevenson SR (2015) From pond slime to rain forest: the evolution of ABA signalling and the acquisition of dehydration tolerance. New Phytol 206(1):5–7

    CAS  PubMed  Google Scholar 

  • Czyzewicz N, Nikonorova N, Meyer MR et al (2016) The growing story of (ARABIDOPSIS) CRINKLY 4. J Exp Bot 67(16):4835–4847

    CAS  PubMed  Google Scholar 

  • Dall'Osto L, Holt NE, Kaligotla S, Fuciman M, Cazzaniga S, Carbonera D, Frank HA, Alric J, Bassi R (2012) Zeaxanthin protects plant photosynthesis by modulating chlorophyll triplet yield in specific light-harvesting antenna subunits. J Biol Chem 287(50):41820–41834

    CAS  PubMed  PubMed Central  Google Scholar 

  • Daszkowska-Golec A, Skubacz A, Sitko K et al (2018) Mutation in barley ERA1 (Enhanced Response to ABA1) gene confers better photosynthesis efficiency in response to drought as revealed by transcriptomic and physiological analysis. Environ Exp Bot 148:12–26

    CAS  Google Scholar 

  • Dill A, Jung HS, Sun TP (2001) The DELLA motif is essential for gibberellin-induced degradation of RGA. Proc Natl Acad Sci U S A 98(24):14162–14167

    CAS  PubMed  PubMed Central  Google Scholar 

  • Eckardt NA (2006) Function of gamma-tubulin in plants. Plant Cell 18(6):1327–1329

    CAS  PubMed Central  Google Scholar 

  • El Zawily AM, Schwarzländer M, Finkemeier I et al (2014) FRIENDLY regulates mitochondrial distribution, fusion, and quality control in Arabidopsis. Plant Physiol 166(2):808–828. https://doi.org/10.1104/pp.114.243824

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, Mitchell SE (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS One 6(5):e19379

    CAS  PubMed  PubMed Central  Google Scholar 

  • Endo T, Shimada T, Nakata Y et al (2017) Abscisic acid affects expression of citrus FT homologs upon floral induction by low temperature in Satsuma mandarin (Citrus unshiu Marc.). Tree Physiol 38:755–771. https://doi.org/10.1093/treephys/tpx145

    Article  CAS  Google Scholar 

  • Fagoaga C, Tadeo FR, Iglesias DJ, Huerta L, Lliso I, Vidal AM, Talon M, Navarro L, García-Martínez JL, Peña L (2007) Engineering of gibberellin levels in citrus by sense and antisense overexpression of a GA 20-oxidase gene modifies plant architecture. J Exp Bot 58(6):1407–1420

    CAS  PubMed  Google Scholar 

  • Goncalves de Albuquerque HY, do Carmo CD, Brito AC et al (2018) Genetic diversity of Manihot esculenta Crantz germplasm based on single-nucleotide polymorphism markers. Ann Appl Biol 173:271–284

    Google Scholar 

  • Guyomarc’h S, Vernoux T, Traas J et al (2004) MGOUN3, an Arabidopsis gene with TetratricoPeptide-repeat-related motifs, regulates meristem cellular organization. J Exp Bot 55(397):673–684

    PubMed  Google Scholar 

  • Huang M, Liu X, Zhou Y et al (2018) BLINK: a package for the next level of genome-wide association studies with both individual and markers in the millions. GigaScience 8(2):Feb 2019, giy154

  • Jiang CJ, Nakajima N, Kondo N (1996) Disruption of microtubules by abscisic acid in guard cells of Vicia faba L. Plant Cell Physiol 37(5):697–701

    CAS  Google Scholar 

  • Jin P, Guo T, Becraft PW (2000) The maize CR4 receptor-like kinase mediates a growth factor-like differentiation response. Genesis 27(3):104–116

    CAS  PubMed  Google Scholar 

  • Kilian A, Huttner E, Wenzyl P et al (2003) The fast and the cheap: SNP and DArT-based whole genome profiling for crop improvement. Tuberosa R, Phillips RL and Gale M (eds.) Proceedings of the international congress “in the wake of the double Helix: from the green revolution to the gene revolution”. Italy. 443-461

  • Kilian A, Wenzl P, Huttner E et al (2012) Diversity arrays technology: a generic genome profiling technology on open platforms. Methods Mol Biol 888:67–89

    PubMed  Google Scholar 

  • Kilian A, Sanewski G, Ko L (2016) The application of DArTseq technology to pineapple. Acta Hortic 1111:181–188

    Google Scholar 

  • Kim S-C, Chapman KD, Blancaflor EB (2010) Fatty acid amide lipid mediators in plants. Plant Sci 178:411–419. https://doi.org/10.1016/j.plantsci.2010.02.017

    Article  CAS  Google Scholar 

  • Kimura Y, Tasaka M, Torii KU et al (2018) ERECTA-family genes coordinate stem cell functions between the epidermal and internal layers of the shoot apical meristem. Development 145(1):56380–56380

    Google Scholar 

  • Kipreos ET, Pagano M (2000) The F-box protein family. Genome Biol 1(5):3002.2-3002.7

    Google Scholar 

  • Kirchhelle C, Chow C-M, Foucart C, Neto H, Stierhof YD, Kalde M, Walton C, Fricker M, Smith RS, Jérusalem A, Irani N, Moore I (2016) The specification of geometric edges by a plant Rab GTPase is an essential cell-patterning principle during organogenesis in Arabidopsis. Dev Cell 36:386–400

    CAS  PubMed  PubMed Central  Google Scholar 

  • Knoch E, Dilokpimol A, Tryfona T, Poulsen CP, Xiong G, Harholt J, Petersen BL, Ulvskov P, Hadi MZ, Kotake T, Tsumuraya Y, Pauly M, Dupree P, Geshi N (2013) A B-glucuronosyltransferase from Arabidopsis thaliana involved in biosynthesis of type II arabinogalactan has a role in cell elongation during seedling growth. Plant J 76(6):1016–1029

    CAS  PubMed  Google Scholar 

  • Kong Y, Zhou G, Abdeen AA, Schafhauser J, Richardson B, Atmodjo MA, Jung J, Wicker L, Mohnen D, Western T, Hahn MG (2013) GALACTURONOSYLTRANSFERASE-LIKE5 is involved in the production of Arabidopsis seed coat mucilage. Plant Physiol 163(3):1203–1217

    CAS  PubMed  PubMed Central  Google Scholar 

  • Krauss B (1949) Anatomy of the vegetative organs of the pineapple, Ananas comosus (L.) MERR. II. The leaf. Bot Gaz 110(3):333–404

    Google Scholar 

  • Lev-Yadun S et al (2018) Differences in flower colors between spiny and non-spiny Asteraceae species: a possible case of aposematism? Flora 239:98–103

    Google Scholar 

  • Li Z, Peers G, Dent RM et al (2016) Evolution of an atypical de-epoxidase for photoprotection in the green lineage. Nat Plants 2(10):16140–16140

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li J, Zhang X, Lu Y et al (2019) Characterization of non-heading mutation in heading Chinese cabbage (Brassica rapa L. ssp. Pekinensis). Front Plant Sci 10(112):1–112. https://doi.org/10.3389/fpls.2019.00112

    Article  Google Scholar 

  • Liu H, Stone SL (2011) E3 ubiquitin ligases and abscisic acid signalling. Plant Signal Behav 6(3):344–348

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu J, Luo M, Yan X, Yu C, Li S (2016a) Characterization of genes coding for galacturonosyltransferase-like (GATL) proteins in rice. Genes Genom 38:917–929. https://doi.org/10.1007/s13258-016-0436-0

    Article  CAS  Google Scholar 

  • Liu X, Huang M, Fan B, Buckler ES, Zhang Z (2016b) Iterative usage of fixed and random effect models for powerful and efficient genome-wide association studies. PLoS Genet 12(2):e1005767. https://doi.org/10.1371/journal.pgen.1005767

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu L, Li C, Song S, Teo ZWN, Shen L, Wang Y, Jackson D, Yu H (2018) FTIP-dependent STM trafficking regulates shoot meristem development in Arabidopsis. Cell Rep 23(6):1879–1890

    CAS  PubMed  Google Scholar 

  • Lu P, Magwanga RO, Kirunga JN et al (2019) Overexpression of cotton a DTX/MATE gene enhances drought, salt, and cold stress tolerance on transgenic Arabidopsis. Front Plant Sci 10(299):1–19. https://doi.org/10.3389/fpls.2019.00299

    Article  Google Scholar 

  • Mauseth JD (1977) Cytokinin- and gibberellic acid-induced effects on the determination and morphogenesis of leaf primordia in Opuntia polyacantha (Cactaceae). Am J Bot 64(3):337–346

    CAS  Google Scholar 

  • Milborrow BV (2001) The pathway of biosynthesis of abscisic acid in vascular plants: a review of the present state of knowledge of ABA biosynthesis. J Exp Bot 52(359):1145–1164

    CAS  PubMed  Google Scholar 

  • Ming R, VanBuren R, Yu Q (2015) The pineapple genome and evolution of CAM photosynthesis. Nat Genet 47:1435–1442

    CAS  PubMed  PubMed Central  Google Scholar 

  • Money D, Gardner K, Migicovsky Z, Schwaninger H, Zhong GY, Myles S (2015) LinkImpute: fast and accurate genotype imputation for non-model organisms. G3-Genes Genom Genet 5(11):2383–2390

    Google Scholar 

  • Munoz-Nortes T, Perez-Perez JM, Ponce MR et al (2017) The ANGULATA7 gene encodes a Dnaj-like zinc finger-domain protein involved in chloroplast function and leaf development in Arabidopsis. Plant J 89:870–884

    CAS  PubMed  Google Scholar 

  • Mutuku JM, Nose A (2012) Changes in the contents of metabolites and enzyme activities in rice plants responding to Rhizoctonia solani Kuhn infection: activation of glycolysis and connection to phenylpropanoid pathway. Plant Cell Physiol 53(6):1017–1032. https://doi.org/10.1093/pcp/pcs047

    Article  CAS  PubMed  Google Scholar 

  • Noble TJ, Tao Y, Mace ES et al (2018) Characterization of linkage disequilibrium and population structure in a mung bean diversity panel. Front Plant Sci 8(2102). https://doi.org/10.3389/fpls.2017.02102

  • O’Connor K, Kilian A, Hayes B, Hardner C, Nock C, Baten A, Alam M, Topp B (2019) Population structure, genetic diversity and linkage disequilibrium in macadamia breeding population using SNP and silicoDArT markers. Tree Genet Genomes 15:24. https://doi.org/10.1007/s11295-019-1331-z

    Article  Google Scholar 

  • Omasheva ME, Pozharsky AS, Smailov BB et al (2017) Genetic diversity of apple cultivars growing in Kazakhastan. Russ J Genet 54(2):176–187

    Google Scholar 

  • Palmer JW, Seymour SM, Diack R (2011) Feathering of 'Doyenne du Comice' pear in the nursery using repeat sprays of benzyladenine and gibberellins. Sci Hortic 130(2):393–397

    CAS  Google Scholar 

  • Paparelli E, Gonzali S, Parlanti S, Novi G, Giorgi FM, Licausi F, Kosmacz M, Feil R, Lunn JE, Brust H, van Dongen J, Steup M, Perata P (2012) Misexpression of a chloroplast aspartyl protease leads to severe growth defects and alters carbohydrate metabolism in Arabidopsis. Plant Physiol 160:1237–1250

    CAS  PubMed  PubMed Central  Google Scholar 

  • Riboni M, Test AR, Galbiati M et al (2016) ABA-dependent control of GIGANTEA signalling enables drought escape via up-regulation of FLOWERING LOCUS T in Arabidopsis thaliana. J Exp Bot 67(22):6309–6322. https://doi.org/10.1093/jxb/erw384

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rosado A, Schapire AL, Bressan RA, Harfouche AL, Hasegawa PM, Valpuesta V, Botella MA (2006) The Arabidopsis tetratricopeptide repeat-containing protein TTL1 is required for osmotic stress responses and abscisic acid sensitivity. Plant Physiol 142:1113–1126

    CAS  PubMed  PubMed Central  Google Scholar 

  • Running MP (2014) The role of lipid post-translational modification in plant developmental processes. Front Plant Sci 5(50):1–9. https://doi.org/10.3389/fpls.2014.00050

    Article  Google Scholar 

  • Sakiyamasogo M, Shibaoka H (1993) Gibberellin A-3 and abscisic-acid cause the reorientation of cortical microtubules in epicotyl cells of the decapitated dwarf pea. Plant Cell Physiol 34(3):431–437

    CAS  Google Scholar 

  • Salas-Munoz S, Rodriguez-Hernandez AA, Ortega-Amaro MA et al (2016) Arabidopsis AtDjA3 null mutant shows increase sensitivity to abscisic acid, salt, and osmotic stress in germination and post-germination stages. Front Plant Sci 7(220):1–11. https://doi.org/10.3389/fpls.2016.00220

    Article  Google Scholar 

  • Sanewski G (2019) The history of pineapple improvement. In: Ming R (ed) Plant genetics and genomics: crops and models. Genetics and Genomics of Pineapple. Springer, Cham. https://doi.org/10.1007/978-3-030-00614-3

    Chapter  Google Scholar 

  • Sanewski GM, Smith MK, Pepper PM et al (2011) Review of genetic improvement of pineapple. Acta Hortic 902:95–108

    Google Scholar 

  • Sanewski G, Ko L, Innes D et al (2017) DArTseq molecular markers for resistance to Phytophthora cinnamomi in pineapple (Ananas comosus L.). Australas Plant Pathol 46(5):499–509

    CAS  Google Scholar 

  • Sanewski G, Coppens d’Eeckenbrugge G, Junghans D (2018) Varieties and breeding. In: Sanewski G, Bartholomew D, Paull R (eds) The pineapple: botany, production and uses, 2nd edn. CABI, Oxfordshire

    Google Scholar 

  • Santos AL, Chaves-Silva S, Yang L et al (2017) Global analysis of the MATE gene family of metabolite transporters in tomato. BMC Plant Biol 17:185–185

    PubMed  PubMed Central  Google Scholar 

  • Segura V, Vilhjalmssom BJ, Platt A et al (2012) An efficient multi-locus mixed-model approach for genome-wide association studies in structured populations. Nat Genet 44(7):825–832. https://doi.org/10.1038/ng.2314

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sekhwal MK, Li P, Lan I, Wang X et al (2015) Disease resistance gene analogs (RGAs) in plants. Int J Mol Sci 16(8):19248–19290

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shi W, Zeng Q, Kunkel BN, Running M (2015) Arabidopsis Rab geranylgeranyltransferases demonstrate redundancy and broad substrate specificity in vitro. J Biol Chem 291(3):1398–1410

    PubMed  PubMed Central  Google Scholar 

  • Shpak ED (2013) Diverse roles of ERECTA family genes in plant development. J Integr Plant Biol 55(12):1238–1250

    CAS  PubMed  Google Scholar 

  • Singleton VL, Gortner WA, Young HY (1960) Carotenoid pigments of pineapple Fruit. I. Acid-catalyzed Isomerization of the Pigments Pineapple Research Institute of Hawaii. Technical paper No. 27. P49–52

  • Smith MK, Ko H-L, Hamill SD, Sanewski GM (2002) Pineapple transformation: Somaclonal variation. Acta Hortic 575:69–74

    Google Scholar 

  • Soares A, Ribeiro Carlton SM, Simoes I (2019) Atypical and nucellin-like aspartic proteases: emerging players in plant developmental processes and stress responses. J Exp Bot 70(7):2059–2076. https://doi.org/10.1093/jxb/erz0.34

    Article  CAS  PubMed  Google Scholar 

  • Somssich M, Je BI, Simon R, Jackson D (2016) CLAVATA-WUSCHEL signaling in the shoot meristem. Development 143(18):3238–3248

    CAS  PubMed  Google Scholar 

  • Song S, Chen Y, Liu L, Wang Y, Bao S, Zhou X, Teo ZW, Mao C, Gan Y, Yu H (2017) OsFTIP1-mediated regulation of florigen transport in rice is negatively regulated by the ubiquitin-like domain kinase OsUbDK gamma 4. Plant Cell 29(3):491–507

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sotta N, Shantikumar L, Sakamoto T et al (2016) TPR5 is involved in directional cell division and is essential for the maintenance of meristem cell organization in Arabidopsis thaliana. J Exp Biol 67(8):2401–2411

    CAS  Google Scholar 

  • Speth EB, Imboden L, Hauck P, Sheng YH (2009) Subcellular localization and functional analysis of the Arabidopsis GTPase RabE. Plant Physiol 149:1824–1837

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sunohara H, Kawai T, Shimizu-Sato S, Sato Y, Sato K, Kitano H (2009) A dominant mutation of TWISTED DWARF 1 encoding an A-tubulin protein causes severe dwarfism and right helical growth in rice. Genes Genet Syst 84:209–218

    CAS  PubMed  Google Scholar 

  • Tang Y, Liu X, Wang J et al (2016) GAPIT version 2: an enhanced integrated tool for genomic association and prediction. Plant Genome 9(2):1–9

    Google Scholar 

  • Teaster ND, Keereetaweep J, Kilaru A et al (2012) Overexpression of fatty acid amide hydrolase induces early flowering in Arabidopsis thaliana. Front Plant Sci 3(32):1–13. https://doi.org/10.3389/fpls.2012.00032

    Article  CAS  Google Scholar 

  • Urasaki N, Goeku S, Kaneshima R, Takamine T, Tarora K, Takeuchi M, Moromizato C, Yonamine K, Hosaka F, Terakami S, Matsumura H, Yamamoto T, Shoda M (2015) Leaf margin phenotype-specific restriction-site-associated DNA-derived markers for pineapple (Ananas comosus L.). Breed Sci 65(3):276–284

    CAS  PubMed  PubMed Central  Google Scholar 

  • Van Raden PM (2008) Efficient methods to compare genomic predictions. J Dairy Sci 91:4414–4423

    Google Scholar 

  • Vos PG, Paulo MJ, Voorips RE et al (2017) Evaluation of LD decay and various LD-decay estimators in simulated and SNP array data of tetraploid potato. Theor Appl Genet 130:123–135

    PubMed  Google Scholar 

  • Wang Q, Tian F, Pan Y, Buckler ES, Zhang Z (2014) A SUPER powerful method for genome wide association study. PLoS One 9(9):e107684

    PubMed  PubMed Central  Google Scholar 

  • Wang B, Li C, Kong X, Li Y, Liu Z, Wang J, Li X, Yang Y (2018) AtARRE, an E3 ubiquitin ligase, negatively regulates ABA signalling in Arabidopsis thaliana. Plant Cell Rep 37:1269–1278. https://doi.org/10.1007/s00299-018-2311-8

    Article  CAS  PubMed  Google Scholar 

  • Wu Y, Luo L, Chen L, Tao X, Huang M, Wang H, Chen Z, Xiao W (2016) Chromosome mapping, molecular cloning and expression analysis of a novel gene response for leaf width in rice. Biochem Biophys Res Commun 480(3):394–401

    CAS  PubMed  Google Scholar 

  • Xu H, Yu Q, Shi Y, Hua X, Tang H, Yang L, Ming R, Zhang J (2018) PGD: pineapple genomics database. Hortic Res 5(1):1–9. https://doi.org/10.1038/s41438-018-0078-2

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang G, Jan A, Komatsu S (2009) Characterization of β-tubulin 4 regulated by gibberellins in rice leaf sheath. Biol Plant 53(3):422–428

    CAS  Google Scholar 

  • Yao X, Xiong W, Ye T, Wu Y (2012) Overexpression of the aspartic protease ASPG1 gene confers drought avoidance in Arabidopsis. J Exp Bot 63(7):2579–2593

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang J and Ming R (2018) Pineapple genomics database. http://pineapple.angiosperms.org/pineapple/html/index.htmlAccessed 30 Dec 2019

  • Zhang Z, Ersov E, Lai CQ et al (2010) Mixed linear model approach adapted for genome-wide association studies. Nat Genet 42(4):355–360

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Zhu H, Pan Y, Yu Y, Luan S, Li L (2014) A DTX/MATE-type transporter facilitates abscisic acid efflux and modulates ABA sensitivity and drought tolerance in Arabidopsis. Mol Plant 7(10):1522–1532. https://doi.org/10.1093/mp/ssu063

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Hafeez MT, Di D et al (2019) Precise control of ABA signalling through post-translational protein modification. Plant Growth Regul 88:99–111

    CAS  Google Scholar 

  • Zhao Y, Liu X, Xu Z, Yang H, Li J (2017) Characterization and enzymatic properties of protein kinase ACR4 from Arabidopsis thaliana. Biochem Biophys Res Commun 489(2):270–274

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The author would like to thank D. Innes and K. O’Connor and the reviewers for their helpful comments on the manuscript.

Funding

The project was funded by Horticulture Innovation Australia Pty Ltd. (Hort Innovation) using voluntary contributions from the Department of Agriculture and Fisheries and matched funds from the Australian Government.

Author information

Authors and Affiliations

  1. Queensland Government, Department of Agriculture and Fisheries, Maroochy Research Facility, 47 Mayers Rd Queensland, Nambour, 4560, Australia

    Garth M. Sanewski

Authors
  1. Garth M. Sanewski
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Garth M. Sanewski.

Additional information

Communicated by: Yann-Rong Lin

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic Supplementary Material

Fig. S1

Linkage decay curve for LG06. A Loess curve line is shown in pink. The LD decay distance is the point where the X axis corresponds with 50% of the vertical fitted curve maximum as shown. (PNG 1474 kb)

High resolution image (TIFF 44062 kb)

Fig. S2

Linkage haploblocks for LG06 (Haploview 4.2). The pink bar covers the significantly associated loci and up to 300 kb either side of SNP positions (13.6–14.7 Mb). R2 = 1 (black), 0 < r2 < 1 (shades of grey), r2 = 0 (white). (PNG 626 kb)

High resolution image (TIF 12153 kb)

Fig. S3

Haploblocks for the significantly associated region on LG06 (Haploview 4.2). R2 = 1 (black), 0 < r2 < 1 (shades of grey), r2 = 0 (white). Matched, significantly associated SNP markers are surrounded by a coloured frame. (PNG 1327 kb)

High resolution image (TIFF 28695 kb)

Fig. S4

Principal components bi-plot for SNP markers (TASSEL 5). The different coloured symbols indicate the different genotype groups. M × C = ‘MD-2’♀ × ‘Smooth Cayenne’♂; C × M = ‘Smooth Cayenne’♀ × ‘MD-2’♂. (PNG 197 kb)

High resolution image (TIFF 39649 kb)

Figs S5

A and B Scree plots (eigenvalues) for SNPs (A) and silicoDArTs (B). The number of principal components used in the analyses are indicated. (PNG 130 kb)

High resolution image (TIFF 23789 kb)

Table S1

Linkage estimate matrix (r2 and D′) for significant, matched SNPs (Haploview 4.2). D′ values are above the diagonal and r2 below. (DOCX 15 kb)

Table S2

Nucleotide sequences for all significantly associated SNPs (trimmed sequences) using three algorithms in GAPIT. Both the reference and SNP sequences are shown. (DOCX 17 kb)

Table S3

Nucleotide sequences for all significantly associated silicoDArT (trimmed sequences) using three algorithms in GAPIT. (DOCX 13 kb)

Table S4

Predominant allele states for only the most highly significant and matched SNP markers in two seedling populations, the two spiny-tip parent cultivars, MD-2 and Smooth Cayenne and ten other unrelated genotypes. The allele states for SNPs are before imputation of null alleles. The ‘Smooth Cayenne’ genome was used as the reference for markers calls. -Log10P is from ECMLM analysis unless only significant using other algorithms; then it relates to MLMM preferentially. Correct, unambiguous allele states according to the seedling data are coloured similarly (spiny yellow; spiny-tip green). Wild, primitive genotypes are coloured blue in the header and pre-Columbian domesticates are coloured pink except for the two parents which are not coloured. 0 = homozygous reference allele; 1 = homozygous SNP allele; 2 = heterozygous. Redsp = Red Spanish, Roxo = Roxo de Tefe, Parg = Parguazensis, F19 = FRF19, F361 = FRF361, F223 = FRF223 and macro = A. macrodontes. (DOCX 17 kb)

Table S5

Predominant allele states for only the most highly significant and matched silicoDArT markers in two seedling populations, the two spiny-tip parent cultivars, MD-2 and Smooth Cayenne and ten other unrelated genotypes. The ‘Smooth Cayenne’ genome was used as the reference for markers calls. -Log10P is from ECMLM analysis unless only significant using other algorithms; then it relates to MLMM preferentially. Correct, unambiguous allele states according to the seedling data are coloured similarly (spiny yellow; spiny-tip green). Wild, primitive genotypes are coloured blue in the header and pre-Columbian domesticates are coloured pink except for the two parents which are not coloured. 0 = absent; 1 = present. Redsp = Red Spanish, Roxo = Roxo de Tefe, Parg = Parguazensis, F19 = FRF19, F361 = FRF361, F223 = FRF223 and macro = A. macrodontes. (DOCX 14 kb)

Table S6

RNAseq data (FPKM) for genes with a strong positive co-expression with zeaxanthin epoxidase (Aco08515.1) from the Pineapple Genomics Database website of Zhang and Ming (2018) (http://pineapple.angiosperms.org/pineapple/html/index.html) as cited by Xu et al. (2018). Data is a mean of eight samples from cultivar MD-2. Leaf tissues progress from the base to the tip such that S1 = basal white, S2 = white, S3 = white/green, S4 = proximal mid-leaf green, S5-distal mid-leaf green and S6 = tip. Only genes with a positive Pearson correlation of ≥0.8 are shown. (DOCX 26 kb)

Table S7

RNAseq data (FPKM) for genes with a strong negative co-expression with zeaxanthin epoxidase (Aco08515.1) from the Pineapple Genomics Database website of Zhang and Ming (2018) (http://pineapple.angiosperms.org/pineapple/html/index.html) as cited by Xu et al. (2018). Data is a mean of eight samples from cultivar MD-2. Leaf tissues progress from the base to the tip such that S1 = basal white, S2 = white, S3 = white/green, S4 = proximal mid-leaf green, S5-distal mid-leaf green and S6 = tip. Only genes with a negative Pearson correlation of ≤ −0.8 are shown. (DOCX 17 kb)

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sanewski, G.M. DArTseq Molecular Markers Associated with the Spiny-Tip Leaf Margin in Pineapple (Ananas comosus L.). Tropical Plant Biol. 13, 91–116 (2020). https://doi.org/10.1007/s12042-019-09245-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12042-019-09245-z

Keywords

search

Navigation