QTL mapping reveals genomic regions for yield based on an incremental tolerance index to drought stress and related agronomic traits in canola
Harsh Raman A F , Rosy Raman A , Ky Mathews B , Simon Diffey C and Phil Salisbury D EA NSW Department of Primary Industries, Wagga Wagga Agricultural Institute, Wagga Wagga, NSW 2650, Australia.
B Centre for Bioinformatics and Biometrics (CBB), National Institute for Applied Statistics Research Australia (NIASRA), University of Wollongong, NSW 2522, Australia.
C Apex Biometry, South Fremantle, WA 6162, Australia.
D Agriculture Victoria, Department of Jobs, Precincts and Regions, Horsham, Vic. 3400, Australia.
E Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Vic. 3010, Australia.
F Corresponding author. Email: harsh.raman@dpi.nsw.gov.au
Crop and Pasture Science 71(6) 562-577 https://doi.org/10.1071/CP20046
Submitted: 14 February 2020 Accepted: 30 April 2020 Published: 16 May 2020
Abstract
Drought stress, especially at the reproductive stage, is a major limiting factor that compromises the productivity and profitability of canola in many regions of the world. Improved genetics for drought tolerance would enable the identification and development of resilient cultivars, resulting in increased canola production. The main objective of the present study was to dissect the genetic basis of seed yield of canola under water-limited conditions. A doubled haploid population derived from a cross between two Australian parental lines, RP04 and Ag-Outback, was evaluated to identify the genetic variation in fractional normalised deviation vegetative index (NDVI), aboveground shoot biomass accumulation, flowering time and plasticity in seed yield under irrigated and rainfed field conditions in two consecutive years. An irrigation treatment was applied at the 50% flowering stage and an incremental drought tolerance index (DTI) was estimated for seed yield. By utilising a genetic linkage map based on 18 851 genome-wide DArTseq markers, we identified 25 genomic regions significantly associated with different traits (logarithm of odds (LOD) ≥ 3), accounting for 5.5–22.3% of the genotypic variance. Three significant genomic regions on chromosomes A06, A10 and C04 were associated with DTI for seed yield. Some of the quantitative trait loci (QTL) were localised in the close proximity of candidate genes involved in traits contributing to drought escape and drought avoidance mechanisms, including FLOWERING LOCUS T (FT) and FLOWERING LOCUS C (FLC). Trait-marker associations identified herein can be validated across diverse environments, and the sequence-based markers may be used in a marker assisted selection breeding strategy to enhance drought tolerance in canola breeding germplasm.
Additional keywords: biomass, Brassica napus, early vigour, NDVI, QTL mapping, response to drought.
References
Adamsen FG, Pinter PJ, Barnes EM, LaMorte RL, Wall GW, Leavitt SW, Kimball BA (1999) Measuring wheat senescence with a digital camera. Crop Science 39, 719–724.| Measuring wheat senescence with a digital camera.Crossref | GoogleScholarGoogle Scholar |
Alexandratos N, Bruinsma J (2012) World agriculture towards 2030/2050: the 2012 revision. ESA Working Paper No. 12–03. pp. 147. FAO, Rome, Italy.
Bailey R (2008) ‘Design of comparative experiments.’ (Cambridge Series in Statistical and Probabilistic Mathematics, Cambridge University Press: Cambridge, UK)
Bond DM, Wilson IW, Dennis ES, Pogson BJ, Jean Finnegan E (2009) VERNALIZATION INSENSITIVE 3 (VIN3) is required for the response of Arabidopsis thaliana seedlings exposed to low oxygen conditions. The Plant Journal 59, 576–587.
| VERNALIZATION INSENSITIVE 3 (VIN3) is required for the response of Arabidopsis thaliana seedlings exposed to low oxygen conditions.Crossref | GoogleScholarGoogle Scholar | 19392705PubMed |
Butler DG, Cullis BR, Gilmour AR, Gogel BJ (2009) ASReml-R reference manual. Release 3.0. Technical report, Queensland Department of Primary Industries, Australia. Available at: http://www.vsni.co.uk/downloads/asreml/release2/doc/asreml-R.pdf (accessed 2 May 2020)
Carlson TN, Ripley DA (1997) On the relation between NDVI, fractional vegetation cover, and leaf area index. Remote Sensing of Environment 62, 241–252.
| On the relation between NDVI, fractional vegetation cover, and leaf area index.Crossref | GoogleScholarGoogle Scholar |
Chalhoub B, Denoeud F, Liu S, Parkin IA, Tang H, Wang X, Chiquet J, Belcram H, Tong C, Samans B, Correa M, Da Silva C, Just J, Falentin C, Koh CS, Le Clainche I, Bernard M, Bento P, Noel B, Labadie K, Alberti A, Charles M, Arnaud D, Guo H, Daviaud C, Alamery S, Jabbari K, Zhao M, Edger PP, Chelaifa H, Tack D, Lassalle G, Mestiri I, Schnel N, Le Paslier MC, Fan G, Renault V, Bayer PE, Golicz AA, Manoli S, Lee TH, Thi VH, Chalabi S, Hu Q, Fan C, Tollenaere R, Lu Y, Battail C, Shen J, Sidebottom CH, Wang X, Canaguier A, Chauveau A, Berard A, Deniot G, Guan M, Liu Z, Sun F, Lim YP, Lyons E, Town CD, Bancroft I, Wang X, Meng J, Ma J, Pires JC, King GJ, Brunel D, Delourme R, Renard M, Aury JM, Adams KL, Batley J, Snowdon RJ, Tost J, Edwards D, Zhou Y, Hua W, Sharpe AG, Paterson AH, Guan C, Wincker P (2014) Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome. Science 345, 950–953.
| Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome.Crossref | GoogleScholarGoogle Scholar | 25146293PubMed |
Condon AG, Richards RA, Rebetzke GJ, Farquhar GD (2002) Improving intrinsic water-use efficiency and crop yield. Crop Science 42, 122–131.
Condon AG, Richards RA, Rebetzke GJ, Farquhar GD (2004) Breeding for high water use efficiency. Journal of Experimental Botany 55, 2447–2460.
| Breeding for high water use efficiency.Crossref | GoogleScholarGoogle Scholar | 15475373PubMed |
Cooper M, Stucker RE, DeLacy IH, Harch BD (1997) Wheat breeding nurseries, target environments, and indirect selection for grain yield. Crop Science 37, 1168–1176.
| Wheat breeding nurseries, target environments, and indirect selection for grain yield.Crossref | GoogleScholarGoogle Scholar |
Cowley RB, Luckett DJ, Moroni JS, Zeleke K, Diffey S (2014) Remote sensing of early vigour in canola germplasm: relationship to grain yield and potential to select for drought tolerance. Crop & Pasture Science 65, 1288–1299.
| Remote sensing of early vigour in canola germplasm: relationship to grain yield and potential to select for drought tolerance.Crossref | GoogleScholarGoogle Scholar |
Craine JM, Ocheltree TW, Nippert JB, Towne EG, Skibbe AM, Kembel SW, Fargione JE (2013) Global diversity of drought tolerance and grassland climate-change resilience. Nature Climate Change 3, 63–67.
| Global diversity of drought tolerance and grassland climate-change resilience.Crossref | GoogleScholarGoogle Scholar |
De Lucia F, Crevillen P, Jones AM, Greb T, Dean C (2008) A PHD-polycomb repressive complex 2 triggers the epigenetic silencing of FLC during vernalization. Proceedings of the National Academy of Sciences of the United States of America 105, 16831–16836.
Dolferus R, Thavamanikumar S, Sangma H, Kleven S, Wallace X, Forrest K, Rebetzke G, Hayden M, Borg L, Smith A, Cullis B (2019) Determining the genetic architecture of reproductive stage drought tolerance in wheat using a correlated trait and correlated marker effect model. G3: Genes|Genomes|Genetics 9, 473–489.
Doyle MR, Bizzell CM, Keller MR, Michaels SD, Song JD, Noh YS, Amasino RM (2005) HUA2 is required for the expression of floral repressors in Arabidopsis thaliana. The Plant Journal 41, 376–385.
| HUA2 is required for the expression of floral repressors in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 15659097PubMed |
Ebine K, Okatani Y, Uemura T, Goh T, Shoda K, Niihama M, Morita MT, Spitzer C, Otegui MS, Nakano A, Ueda T (2008) A SNARE complex unique to seed plants is required for protein storage vacuole biogenesis and seed development of Arabidopsis thaliana. The Plant Cell 20, 3006–3021.
| A SNARE complex unique to seed plants is required for protein storage vacuole biogenesis and seed development of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 18984676PubMed |
El-Soda M, Boer MP, Bagheri H, Hanhart CJ, Koornneef M, Aarts MGM (2014) Genotype-environment interactions affecting preflowering physiological and morphological traits of Brassica rapa grown in two watering regimes. Journal of Experimental Botany 65, 697–708.
| Genotype-environment interactions affecting preflowering physiological and morphological traits of Brassica rapa grown in two watering regimes.Crossref | GoogleScholarGoogle Scholar | 24474811PubMed |
Fischer RA, Rees D, Sayre KD, Lu ZM, Condon AG, Larque SA (1998) Wheat yield progress associated with higher stomatal conductance and photosynthetic rate, and cooler canopies. Crop Science 38, 1467–1475.
| Wheat yield progress associated with higher stomatal conductance and photosynthetic rate, and cooler canopies.Crossref | GoogleScholarGoogle Scholar |
Fletcher RS, Mullen JL, Heiliger A, McKay JK (2015) QTL analysis of root morphology, flowering time, and yield reveals trade-offs in response to drought in Brassica napus. Journal of Experimental Botany 66, 245–256.
| QTL analysis of root morphology, flowering time, and yield reveals trade-offs in response to drought in Brassica napus.Crossref | GoogleScholarGoogle Scholar | 25371500PubMed |
Fletcher RS, Herrmann D, Mullen JL, Li Q, Schrider DR, Price N, Lin J, Grogan K, Kern A, McKay JK (2016) Identification of polymorphisms associated with drought adaptation QTL in Brassica napus by resequencing. G3: Genes|Genomes|Genetics 6, 793–803.
| Identification of polymorphisms associated with drought adaptation QTL in Brassica napus by resequencing.Crossref | GoogleScholarGoogle Scholar | 26801646PubMed |
Franks SJ, Sim S, Weis AE (2007) Rapid evolution of flowering time by an annual plant in response to a climate fluctuation. Proceedings of the National Academy of Sciences of the United States of America 104, 1278–1282.
| Rapid evolution of flowering time by an annual plant in response to a climate fluctuation.Crossref | GoogleScholarGoogle Scholar | 17220273PubMed |
Gilmour AR, Cullis BR, Verbyla A, Nas P (1997) Accounting for natural and extraneous variation in the analysis of field experiments. Journal of Agricultural, Biological, & Environmental Statistics 2, 269–293.
| Accounting for natural and extraneous variation in the analysis of field experiments.Crossref | GoogleScholarGoogle Scholar |
González CV, Ibarra SE, Piccoli PN, Botto JF, Boccalandro HE (2012) Phytochrome B increases drought tolerance by enhancing ABA sensitivity in Arabidopsis thaliana. Plant, Cell & Environment 35, 1958–1968.
| Phytochrome B increases drought tolerance by enhancing ABA sensitivity in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
Hall AE, Richards RA, Condon AG, Wright GC, Farquhar GD (2010) Carbon isotope discrimination and plant breeding. In ‘Plant breeding reviews. Vol. 12’. (Ed. J Janick) pp. 81–113. Available at:
Hatzig SV, Frisch M, Breuer F, Nesi N, Ducournau S, Wagner M-H, Leckband G, Abbadi A, Snowdon RJ (2015) Genome-wide association mapping unravels the genetic control of seed germination and vigor in Brassica napus. Frontiers in Plant Science 6, 221
| Genome-wide association mapping unravels the genetic control of seed germination and vigor in Brassica napus.Crossref | GoogleScholarGoogle Scholar | 25914704PubMed |
Holman TJ, Jones PD, Russell L, Medhurst A, Úbeda Tomás S, Talloji P, Marquez J, Schmuths H, Tung S-A, Taylor I, Footitt S, Bachmair A, Theodoulou FL, Holdsworth MJ (2009) The N-end rule pathway promotes seed germination and establishment through removal of ABA sensitivity in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 106, 4549–4554.
| The N-end rule pathway promotes seed germination and establishment through removal of ABA sensitivity in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 19255443PubMed |
Holzapfel CB, Lafond GP, Brandt SA, Bullock PR, Irvine RB, Morrison MJ, May WE, James DC (2009) Estimating canola (Brassica napus L.) yield potential using an active optical sensor. Canadian Journal of Plant Science 89, 1149–1160.
| Estimating canola (Brassica napus L.) yield potential using an active optical sensor.Crossref | GoogleScholarGoogle Scholar |
Jean Finnegan E, Bond DM, Buzas DM, Goodrich J, Helliwell CA, Tamada Y, Yun JY, Amasino RM, Dennis ES (2011) Polycomb proteins regulate the quantitative induction of VERNALIZATION INSENSITIVE 3 in response to low temperatures. The Plant Journal 65, 382–391.
| Polycomb proteins regulate the quantitative induction of VERNALIZATION INSENSITIVE 3 in response to low temperatures.Crossref | GoogleScholarGoogle Scholar | 21265892PubMed |
Lemerle D, Smith A, Verbeek B, Eric K, Lockley P, Martin P (2006) Incremental crop tolerance to weeds: a measure for selecting competitive ability in Australian wheats. Euphytica 149, 85–95.
| Incremental crop tolerance to weeds: a measure for selecting competitive ability in Australian wheats.Crossref | GoogleScholarGoogle Scholar |
Liu L, Zhou Y, Zhou G, Ye RJ, Zhao L, Li XH, Lin YJ (2008) Identification of early senescence-associated genes in rice flag leaves. Plant Molecular Biology 67, 37–55.
| Identification of early senescence-associated genes in rice flag leaves.Crossref | GoogleScholarGoogle Scholar | 18330710PubMed |
Long Y, Shi J, Qiu D, Li R, Zhang C, Wang J, Hou J, Zhao J, Shi L, Park B-S, Choi SR, Lim YP, Meng J (2007) Flowering time quantitative trait loci analysis of oilseed brassica in multiple environments and genomewide alignment with Arabidopsis. Genetics 177, 2433–2444.
| Flowering time quantitative trait loci analysis of oilseed brassica in multiple environments and genomewide alignment with Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 18073439PubMed |
Mailer RJ, Cornish PS (1987) Effects of water stress on glucosinolates and oil content in the seeds of rape (Brassica napus L.) and turnip rape (Brassica rapa L. var. sylvestris (Lam.) Briggs). Australian Journal of Experimental Agriculture 27, 707–711.
| Effects of water stress on glucosinolates and oil content in the seeds of rape (Brassica napus L.) and turnip rape (Brassica rapa L. var. sylvestris (Lam.) Briggs).Crossref | GoogleScholarGoogle Scholar |
Mrode RA (2005) ‘Linear models for the prediction of animal breeding values.’ 2nd edn.’ (CABI Publishing: Wallingford, UK)
Nelson MN, Rajasekaran R, Smith A, Chen S, Beeck CP, Siddique KHM, Cowling WA (2014) Quantitative trait loci for thermal time to flowering and photoperiod responsiveness discovered in summer annual-type Brassica napus L. PLoS One 9,
| Quantitative trait loci for thermal time to flowering and photoperiod responsiveness discovered in summer annual-type Brassica napus L.Crossref | GoogleScholarGoogle Scholar | 25061822PubMed |
R Core Team (2013) ‘R: a language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna, Austria)
Raman H, Raman R, Coombes N, Song J, Prangnell R, Bandaranayake C, Tahira R, Sundaramoorthi V, Killian A, Meng J, Dennis ES, Balasubramanian S (2016a) Genome-wide association analyses reveal complex genetic architecture underlying natural variation for flowering time in canola. Plant, Cell & Environment 39, 1228–1239.
| Genome-wide association analyses reveal complex genetic architecture underlying natural variation for flowering time in canola.Crossref | GoogleScholarGoogle Scholar |
Raman R, Diffey S, Carling J, Cowley R, Kilian A, Luckett D, Raman H (2016b) Quantitative genetic analysis of yield in an Australian Brassica napus doubled haploid population. Crop & Pasture Science 67, 298–307.
| Quantitative genetic analysis of yield in an Australian Brassica napus doubled haploid population.Crossref | GoogleScholarGoogle Scholar |
Raman H, Raman R, Qiu Y, Yadav AS, Sureshkumar S, Borg L, Rohan M, Wheeler D, Owen O, Menz I, Balasubramanian S (2019a) GWAS hints at pleiotropic roles for FLOWERING LOCUS T in flowering time and yield-related traits in canola. BMC Genomics 20, 636
| GWAS hints at pleiotropic roles for FLOWERING LOCUS T in flowering time and yield-related traits in canola.Crossref | GoogleScholarGoogle Scholar | 31387521PubMed |
Raman H, Uppal RK, Raman R (2019b) Genetic solutions to improve resilience of canola to climate change. In ‘Genomic designing of climate-smart oilseed crops’. (Ed. C Kole) pp. 75–131. (Springer International Publishing: Cham, Switzerland)
Raman R, Diffey S, Barbulescu DM, Coombes N, Luckett D, Salisbury P, Cowley R, Marcroft S, Raman H (2020) Genetic and physical mapping of loci for resistance to blackleg disease in canola (Brassica napus L.). Scientific Reports 10, 4416
| Genetic and physical mapping of loci for resistance to blackleg disease in canola (Brassica napus L.).Crossref | GoogleScholarGoogle Scholar | 32157120PubMed |
Rebetzke GJ, Condon AG, Richards RA, Farquhar GD (2002) Selection for reduced carbon-isotope discrimination increases aerial biomass and grain yield of rainfed bread wheat. Crop Science 42, 739–745.
| Selection for reduced carbon-isotope discrimination increases aerial biomass and grain yield of rainfed bread wheat.Crossref | GoogleScholarGoogle Scholar |
Regan KL, Siddique KHM, Turner NC, Whan BR (1992) Potential for increasing early vigour and total biomass in spring wheat. II Characteristics associated with early vigour. Australian Journal of Agricultural Research 43, 541–553.
| Potential for increasing early vigour and total biomass in spring wheat. II Characteristics associated with early vigour.Crossref | GoogleScholarGoogle Scholar |
Regan KL, Siddique KHM, Tennant D, Abrecht DG (1997) Grain yield and water use efficiency of early maturing wheat in low rainfall Mediterranean environments. Australian Journal of Agricultural Research 48, 595–604.
| Grain yield and water use efficiency of early maturing wheat in low rainfall Mediterranean environments.Crossref | GoogleScholarGoogle Scholar |
Reina JJ, Guerrero C, Heredia A (2007) Isolation, characterization, and localization of AgaSGNH cDNA: a new SGNH-motif plant hydrolase specific to Agave americana L. leaf epidermis. Journal of Experimental Botany 58, 2717–2731.
| Isolation, characterization, and localization of AgaSGNH cDNA: a new SGNH-motif plant hydrolase specific to Agave americana L. leaf epidermis.Crossref | GoogleScholarGoogle Scholar | 17609535PubMed |
Riboni M, Galbiati M, Tonelli C, Conti L (2013) GIGANTEA enables drought escape response via abscisic acid-dependent activation of the florigens and SUPPRESSOR OF OVEREXPRESSION OF CONSTANS1. Plant Physiology 162, 1706–1719.
| GIGANTEA enables drought escape response via abscisic acid-dependent activation of the florigens and SUPPRESSOR OF OVEREXPRESSION OF CONSTANS1.Crossref | GoogleScholarGoogle Scholar | 23719890PubMed |
Richards RA, Thurling N (1978) Variation between and within species of rapeseed (Brassica campestris and B. napus) in response to drought stress. II Growth and development under natural drought stresses. Australian Journal of Agricultural Research 29, 479–490.
| Variation between and within species of rapeseed (Brassica campestris and B. napus) in response to drought stress. II Growth and development under natural drought stresses.Crossref | GoogleScholarGoogle Scholar |
Schmalenbach I, Zhang L, Reymond M, Jiménez-Gómez JM (2014) The relationship between flowering time and growth responses to drought in the Arabidopsis Landsberg erecta × Antwerp-1 population. Frontiers in Plant Science 5, 609
| The relationship between flowering time and growth responses to drought in the Arabidopsis Landsberg erecta × Antwerp-1 population.Crossref | GoogleScholarGoogle Scholar | 25426126PubMed |
Shi JQ, Li RY, Qiu D, Jiang CC, Long Y, Morgan C, Bancroft I, Zhao JY, Meng JL (2009) Unraveling the complex trait of crop yield with quantitative trait loci mapping in Brassica napus. Genetics 182, 851–861.
| Unraveling the complex trait of crop yield with quantitative trait loci mapping in Brassica napus.Crossref | GoogleScholarGoogle Scholar |
Sinaki JM, Heravan EM, Rad AS, Noormohammadi GH, Zarei GH (2007) The effects of water deficit during growth stages of canola (Brassica napus L.). American-Eurasian Journal of Agricultural & Environmental Sciences 2, 417–422.
Srivastava AC, Ramos-Parra PA, Bedair M, Robledo-Hernandez AL, Tang Y, Sumner LW, Diaz de la Garza RI, Blancaflor EB (2011) The folylpolyglutamate synthetase plastidial isoform is required for postembryonic root development in Arabidopsis. Plant Physiology 155, 1237–1251.
| The folylpolyglutamate synthetase plastidial isoform is required for postembryonic root development in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 21233333PubMed |
Tesfamariam EH, Annandale JG, Steyn JM (2010) Water stress effects on winter canola growth and yield. Agronomy Journal 102, 658–666.
| Water stress effects on winter canola growth and yield.Crossref | GoogleScholarGoogle Scholar |
Tyagi S, Mazumdar PA, Mayee P, Shivaraj SM, Anand S, Singh A, Madhurantakam C, Sharma P, Das S, Kumar A, Singh A (2018) Natural variation in Brassica FT homeologs influences multiple agronomic traits including flowering time, silique shape, oil profile, stomatal morphology and plant height in B. juncea. Plant Science 277, 251–266.
| Natural variation in Brassica FT homeologs influences multiple agronomic traits including flowering time, silique shape, oil profile, stomatal morphology and plant height in B. juncea.Crossref | GoogleScholarGoogle Scholar | 30466591PubMed |
Verbyla AP, Cullis BR, Thompson R (2007) The analysis of QTL by simultaneous use of the full linkage map. Theoretical and Applied Genetics 116, 95–111.
| The analysis of QTL by simultaneous use of the full linkage map.Crossref | GoogleScholarGoogle Scholar | 17952402PubMed |
Wood CC, Robertson M, Tanner G, Peacock WJ, Dennis ES, Helliwell CA (2006) The Arabidopsis thaliana vernalization response requires a polycomb-like protein complex that also includes VERNALIZATION INSENSITIVE 3. Proceedings of the National Academy of Sciences of the United States of America 103, 14631–14636.