Multivariate associations of flavonoid and biomass accumulation in white clover (Trifolium repens) under drought
Wouter L. Ballizany A C , Rainer W. Hofmann A , M. Z. Zulfiqhar Jahufer B and Brent A. Barrett BA Faculty of Agriculture and Life Sciences, Lincoln University, PO Box 84, Lincoln 7608, New Zealand.
B AgResearch Grasslands Research Centre, PO Box 11008, Palmerston North 4442, New Zealand.
C Corresponding author. Email: wouter.ballizany@gmail.com
Functional Plant Biology 39(2) 167-177 https://doi.org/10.1071/FP11193
Submitted: 29 August 2011 Accepted: 25 November 2011 Published: 18 January 2012
Abstract
White clover (Trifolium repens L.) is an important pasture legume in temperate regions, but growth is often strongly reduced under summer drought. Cloned individuals from a full-sib progeny of a pair cross between two phenotypically distinct white clover populations were exposed to water deficit in pots under outdoor conditions for 9 weeks, while control pots were maintained at field capacity. Water deficit decreased leaf water potential by more than 50% overall, but increased the levels of the flavonol glycosides of quercetin (Q) and the ratio of quercetin and kaempferol glycosides (QKR) by 111% and by 90%, respectively. Water deficit reduced dry matter (DM) by 21%, with the most productive genotypes in the controls showing the greatest proportional reduction. The full-sib progeny displayed a significant increase in the root : shoot ratio by 53% under water deficit. Drought-induced changes in plant morphology were associated with changes in Q, but not kaempferol (K) glycosides. The genotypes with high QKR levels reduced their DM production least under water deficit and increased their Q glycoside levels and QKR most. These data show, at the individual genotype level, that increased Q glycoside accumulation in response to water deficit stress can be positively associated with retaining higher levels of DM production.
Additional keywords: abiotic stress, kaempferol, quercetin, secondary metabolism.
References
Agati G, Tattini M (2010) Multiple functional roles of flavonoids in photoprotection. New Phytologist 186, 786–793.| Multiple functional roles of flavonoids in photoprotection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXotVWhtLc%3D&md5=8757879ccca8c92b77ddf84e2c7b3d42CAS |
Agati G, Stefano G, Biricolti S, Tattini M (2009) Mesophyll distribution of ‘antioxidant’ flavonoid glycosides in Ligustrum vulgare leaves under contrasting sunlight irradiance. Annals of Botany 104, 853–861.
| Mesophyll distribution of ‘antioxidant’ flavonoid glycosides in Ligustrum vulgare leaves under contrasting sunlight irradiance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlKisrjK&md5=c4adbab63f087f16f9ee4424e26c96d8CAS |
Agati G, Biricolti S, Guidi L, Ferrini F, Fini A, Tattini M (2011) The biosynthesis of flavonoids is enhanced similarly by UV radiation and root zone salinity in L. vulgare leaves. Journal of Plant Physiology 168, 204–212.
| The biosynthesis of flavonoids is enhanced similarly by UV radiation and root zone salinity in L. vulgare leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhs1ajtbjE&md5=0593b1ebfc9ae9e96cb7593207769558CAS |
Allen RG, Pereira LS, Raes D, Smith M (1998) Crop evapotranspiration: guidelines for computing crop water requirements. FAO irrigation and drainage paper, 56, xxvi, 300.
Barbour M, Caradus JR, Woodfield DR, Silvester WB (1996) Water stress and water use efficiency of ten white clover cultivars. In ‘White Clover: New Zealand’s Competitive Edge’ Joint symposium, Lincoln University, New Zealand, 21–22 November, 1995, pp.159–162.
Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Critical Reviews in Plant Sciences 24, 23–58.
| Drought and salt tolerance in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXis12ns7c%3D&md5=12559ef8c57d97b58991c497d00e0aa5CAS |
Blum A (2005) Drought resistance, water-use efficiency, and yield potential – are they compatible, dissonant, or mutually exclusive? Australian Journal of Agricultural Research 56, 1159–1168.
| Drought resistance, water-use efficiency, and yield potential – are they compatible, dissonant, or mutually exclusive?Crossref | GoogleScholarGoogle Scholar |
Bray EA (1997) Plant responses to water deficit. Trends in Plant Science 2, 48–54.
| Plant responses to water deficit.Crossref | GoogleScholarGoogle Scholar |
Brown DE, Rashotte AM, Murphy AS, Normanly J, Tague BW, Peer WA, Taiz L, Muday GK (2001) Flavonoids act as negative regulators of auxin transport in vivo in Arabidopsis. Plant Physiology 126, 524–535.
| Flavonoids act as negative regulators of auxin transport in vivo in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXks1Gnu7s%3D&md5=ae85529f4e491252c5005df09a9c7b69CAS |
Buer CS, Imin N, Djordjevic MA (2010) Flavonoids: new roles for old molecules. Journal of Integrative Plant Biology 52, 98–111.
| Flavonoids: new roles for old molecules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXitVOhsLc%3D&md5=4a183e14c90c28a6dba39c8ee7791f13CAS |
Burr EJ (1968) Cluster sorting with mixed character types. I. Standardization of character values. Australian Computer Journal 1, 97–99.
Burr EJ (1970) Cluster sorting with mixed character types. II. Fusion strategies. Australian Computer Journal 2, 98–103.
Caradus JR, Woodfield DR (1998) Genetic control of adaptive root characteristics in white clover. Plant and Soil 200, 63–69.
| Genetic control of adaptive root characteristics in white clover.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXktVKktLc%3D&md5=a17014a7e442989f8a4ba3c84a1110c4CAS |
Chaves MM, Pereira JS, Maroco J, Rodrigues ML, Ricardo CPP, Osorio ML, Carvalho I, Faria T, Pinheiro C (2002) How plants cope with water stress in the field. Photosynthesis and growth. Annals of Botany 89, 907–916.
| How plants cope with water stress in the field. Photosynthesis and growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlsVeitb4%3D&md5=316aa2ecf680d14952ef221702ad2853CAS |
Cooper M, DeLacy IH (1994) Relationships among analytical methods used to study genotypic variation and genotype-by-environment interaction in plant breeding multi-environment experiments. Theoretical and Applied Genetics 88, 561–572.
| Relationships among analytical methods used to study genotypic variation and genotype-by-environment interaction in plant breeding multi-environment experiments.Crossref | GoogleScholarGoogle Scholar |
Czemmel S, Stracke R, Weisshaar B, Cordon N, Harris NN, Walker AR, Robinson SP, Bogs J (2009) The grapevine R2R3-MYB transcription factor VvMYBF1 regulates flavonol synthesis in developing grape berries. Plant Physiology 151, 1513–1530.
| The grapevine R2R3-MYB transcription factor VvMYBF1 regulates flavonol synthesis in developing grape berries.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVCjsbbO&md5=27e7e69768b359e7c368592261fd0890CAS |
DeLacy IH (1981) Cluster analysis for the interpretation of genotype by environment interaction. In ‘Interpretation of plant response and adaptation to agricultural environments.’ (Eds DE Byth, VE Mungomery) pp. 277–292. (Australian Institute of Agricultural Science and Technology: Curtin, ACT)
Dong MW (2006) ‘Modern HPLC for practicing scientists.’ (Wiley: Hoboken, NJ)
Falconer DS, Mackay TFC (1996) ‘Introduction to quantitative genetics.’ 4th edn. (Longman: Harlow, England)
Fiorentino A, D’Abrosca B, Pacifico S, Golino A, Mastellone C, Oriano P, Monaco P (2007) Reactive oxygen species scavenging activity of flavone glycosides from Melilotus neapolitana. Molecules (Basel, Switzerland) 12, 263–270.
| Reactive oxygen species scavenging activity of flavone glycosides from Melilotus neapolitana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXivVOhtrY%3D&md5=c9a4c9ec783dbe1e79bc14085dc9bba0CAS |
Fox PN, Rosielle AA (1982) Reducing the influence of environmental main-effects on pattern-analysis of plant-breeding environments. Euphytica 31, 645–656.
| Reducing the influence of environmental main-effects on pattern-analysis of plant-breeding environments.Crossref | GoogleScholarGoogle Scholar |
Francis GS, Kemp RA (1990) Morphological and hydraulic properties of a silt loam soil in New Zealand as affected by cropping history. Soil Use and Management 6, 145–151.
| Morphological and hydraulic properties of a silt loam soil in New Zealand as affected by cropping history.Crossref | GoogleScholarGoogle Scholar |
Gao J, Huang H, Cheng H (2008) Quercetin promotes auxin transport in Arabidopsis thaliana. Agricultural Science & Technology - Hunan 9, 152–156.
Gerhardt KE, Lampi MA, Greenberg BM (2008) The effects of far-red light on plant growth and flavonoid accumulation in Brassica napus in the presence of ultraviolet B radiation. Photochemistry and Photobiology 84, 1445–1454.
| The effects of far-red light on plant growth and flavonoid accumulation in Brassica napus in the presence of ultraviolet B radiation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVWkt7rN&md5=98d86ee4296cf06e9952ee0401c0e261CAS |
Grieu P, Robin C, Guckert A (1995) Effect of drought on photosynthesis in Trifolium repens – maintenance of photosystem-II efficiency photosynthesis. Plant Physiology and Biochemistry 33, 19–24.
Grime JP (2001) ‘Plant strategies, vegetation processes, and ecosystem properties.’ 2nd edn. (Wiley: New York)
Hernandez I, Alegre L, Munne-Bosch S (2004) Drought-induced changes in flavonoids and other low molecular weight antioxidants in Cistus clusii grown under Mediterranean field conditions. Tree Physiology 24, 1303–1311.
Hewett JE, Moeschberger M (1985) Change over baseline vs percent change over baseline. Biometrics 41, 582
Hofmann RW, Campbell BD (2011) Response of Trifolium repens to UV-B radiation: morphological links to plant productivity and water availability. Plant Biology 13, 896–901.
| Response of Trifolium repens to UV-B radiation: morphological links to plant productivity and water availability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlyku7fJ&md5=baf4a646d1a8f16b0beacfcf733f06b0CAS |
Hofmann RW, Jahufer MZZ (2011) Tradeoff between biomass and flavonoid accumulation in white clover reflects contrasting plant strategies. PLOS One 6, e18949
| Tradeoff between biomass and flavonoid accumulation in white clover reflects contrasting plant strategies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXlt1aitr4%3D&md5=510a0bd1203e0bc6d2309988c2eb5729CAS |
Hofmann RW, Swinny EE, Bloor SJ, Markham KR, Ryan KG, Campbell BD, Jordan BR, Fountain DW (2000) Responses of nine Trifolium repens L. populations to ultraviolet-B radiation: Differential flavonol glycoside accumulation and biomass production. Annals of Botany 86, 527–537.
| Responses of nine Trifolium repens L. populations to ultraviolet-B radiation: Differential flavonol glycoside accumulation and biomass production.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmtVOqsrg%3D&md5=fc4bb4ef6830749db94d36c412fe6901CAS |
Hofmann RW, Campbell BD, Fountain DW, Jordan BR, Greer DH, Hunt DY, Hunt CL (2001) Multivariate analysis of intraspecific responses to UV-B radiation in white clover (Trifolium repens L.). Plant, Cell & Environment 24, 917–927.
| Multivariate analysis of intraspecific responses to UV-B radiation in white clover (Trifolium repens L.).Crossref | GoogleScholarGoogle Scholar |
Hofmann RW, Campbell BD, Bloor SJ, Swinny EE, Markham KR, Ryan KG, Fountain DW (2003) Responses to UV-B radiation in Trifolium repens L. – physiological links to plant productivity and water availability. Plant, Cell & Environment 26, 603–612.
| Responses to UV-B radiation in Trifolium repens L. – physiological links to plant productivity and water availability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjsl2rurk%3D&md5=156c4d77f45d2f68534f0f8c97037764CAS |
Hofmann RW, Lin W, Stilwell SA, Lucas RJ (2007) Comparison of drought resistance in strawberry clover and white clover. Proceedings of the New Zealand Grassland Association 69, 219–222.
Humphreys MW, Yadav RS, Cairns AJ, Turner LB, Humphreys J, Skot L (2006) A changing climate for grassland research. New Phytologist 169, 9–26.
| A changing climate for grassland research.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVygt7k%3D&md5=f9c4925cb3f8c80307e662762144f407CAS |
Jahufer MZZ, Cooper M, Lane LA (1995) Variation among low rainfall white clover (Trifolium repens L) accessions for morphological attributes and herbage yield. Australian Journal of Experimental Agriculture 35, 1109–1116.
| Variation among low rainfall white clover (Trifolium repens L) accessions for morphological attributes and herbage yield.Crossref | GoogleScholarGoogle Scholar |
Jahufer MZZ, Cooper M, Harch BD (1997) Pattern analysis of the diversity of morphological plant attributes and herbage yield in a world collection of white clover (Trifolium repens L) germplasm characterised in a summer moisture stress environment of Australia. Genetic Resources and Crop Evolution 44, 289–300.
| Pattern analysis of the diversity of morphological plant attributes and herbage yield in a world collection of white clover (Trifolium repens L) germplasm characterised in a summer moisture stress environment of Australia.Crossref | GoogleScholarGoogle Scholar |
Knowles IM, Fraser TJ, Daly MJ (2003) White clover: loss in drought and subsequent recovery. In ‘Legumes for dryland pastures’. Proceedings of a New Zealand Grassland Association (Inc.) Symposium held at Lincoln University, 18–19 November, 2003, pp. 37–41.
Kuhn BM, Geisler M, Bigler L, Ringli C (2011) Flavonols accumulate asymmetrically and affect auxin transport in Arabidopsis. Plant Physiology 156, 585–595.
| Flavonols accumulate asymmetrically and affect auxin transport in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnvFWrsLY%3D&md5=ea36574690ea6266fa3dc0d5d2eef1c2CAS |
Lewis D, Bradley M, Bloor S, Swinny E, Deroles S, Winefield C, Davies K (2006) Altering expression of the flavonoid 3′-hydroxylase gene modified flavonol ratios and pollen germination in transgenic Mitchell petunia plants. Functional Plant Biology 33, 1141–1152.
| Altering expression of the flavonoid 3′-hydroxylase gene modified flavonol ratios and pollen germination in transgenic Mitchell petunia plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1OgsLbF&md5=e2fe180fb4f5192e839944e122b11730CAS |
Lewis DR, Ramirez MV, Miller ND, Vallabhaneni P, Ray WK, Helm RF, Winkel BSJ, Muday GK (2011) Auxin and ethylene induce flavonol accumulation through distinct transcriptional networks. Plant Physiology 156, 144–164.
| Auxin and ethylene induce flavonol accumulation through distinct transcriptional networks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmsVWgt74%3D&md5=37360f070fd7a39f48bb382c0d3b093dCAS |
Markham KR (1982) ‘Techniques of flavonoid identification.’ (Academic Press: London)
Mathesius U, Schlaman HRM, Spaink HP, Sautter C, Rolfe BG, Djordjevic MA (1998) Auxin transport inhibition precedes root nodule formation in white clover roots and is regulated by flavonoids and derivatives of chitin oligosaccharides. The Plant Journal 14, 23–34.
| Auxin transport inhibition precedes root nodule formation in white clover roots and is regulated by flavonoids and derivatives of chitin oligosaccharides.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjtV2is7o%3D&md5=c9a51e7222e618fd3e51d195f542525cCAS |
Mehrtens F, Kranz H, Bednarek P, Weisshaar B (2005) The Arabidopsis transcription factor MYB12 is a flavonol-specific regulator of phenylpropanoid biosynthesis. Plant Physiology 138, 1083–1096.
| The Arabidopsis transcription factor MYB12 is a flavonol-specific regulator of phenylpropanoid biosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmtVejsLg%3D&md5=37bcbff0238f52fd4aeea5edf47e483bCAS |
Olsen H, Aaby K, Borge GIA (2010) Characterization, quantification, and yearly variation of the naturally occurring polyphenols in a common red variety of curly kale (Brassica oleracea L. convar. acephala var. sabellica cv. ‘Redbor’). Journal of Agricultural and Food Chemistry 58, 11 346–11 354.
| Characterization, quantification, and yearly variation of the naturally occurring polyphenols in a common red variety of curly kale (Brassica oleracea L. convar. acephala var. sabellica cv. ‘Redbor’).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht12gsb%2FJ&md5=2b9bfbeb3a25750a1c3580646d6a07a1CAS |
Piepho HP, Mohring J, Melchinger AE, Buchse A (2008) BLUP for phenotypic selection in plant breeding and variety testing. Euphytica 161, 209–228.
| BLUP for phenotypic selection in plant breeding and variety testing.Crossref | GoogleScholarGoogle Scholar |
Reddy AR, Chaitanya KV, Vivekanandan M (2004) Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants. Journal of Plant Physiology 161, 1189–1202.
| Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhvFegtA%3D%3D&md5=f18238b3ad396e1ca5ce5c1e89c6eceaCAS |
Rozema J, van de Staaij J, Bjorn LO, Caldwell M (1997) UV-B as an environmental factor in plant life: stress and regulation. Trends in Ecology & Evolution 12, 22–28.
| UV-B as an environmental factor in plant life: stress and regulation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7itFGrsw%3D%3D&md5=b69d9b9a3b361be2abfbb2542cb49230CAS |
Ryan KG, Swinny EE, Markham KR, Winefield C (2002) Flavonoid gene expression and UV photoprotection in transgenic and mutant Petunia leaves. Phytochemistry 59, 23–32.
| Flavonoid gene expression and UV photoprotection in transgenic and mutant Petunia leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXpt1aitLs%3D&md5=081f682713e378f6a327a611e7e79a47CAS |
Sanderson MA, Byers RA, Skinner RH, Elwinger GF (2003) Growth and complexity of white clover stolons in response to biotic and abiotic stress. Crop Science 43, 2197–2205.
| Growth and complexity of white clover stolons in response to biotic and abiotic stress.Crossref | GoogleScholarGoogle Scholar |
Scalabrelli G, Saracini E, Remorini D, Massai R, Tattini M (2007) Changes in leaf phenolic compounds in two grapevine varieties (Vitis vinifera L.) grown in different water conditions. In ‘Proceedings of the International Workshop on Advances in Grapevine and Wine Research, Venosa, Italy, 15–17 September 2005.’ pp. 295–299.
Smith JL, Burritt DJ, Bannister P (2000) Shoot dry weight, chlorophyll and UV-B-absorbing compounds as indicators of a plant’s sensitivity to UV-B radiation. Annals of Botany 86, 1057–1063.
| Shoot dry weight, chlorophyll and UV-B-absorbing compounds as indicators of a plant’s sensitivity to UV-B radiation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXot1Kku70%3D&md5=34aaed1a1fea2bc4b9856f727b5ebb9bCAS |
Stracke R, Ishihara H, Barsch GHA, Mehrtens F, Niehaus K, Weisshaar B (2007) Differential regulation of closely related R2R3-MYB transcription factors controls flavonol accumulation in different parts of the Arabidopsis thaliana seedling. The Plant Journal 50, 660–677.
| Differential regulation of closely related R2R3-MYB transcription factors controls flavonol accumulation in different parts of the Arabidopsis thaliana seedling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmt1Cjtbc%3D&md5=d6b055e925c7c85789e960286c95665bCAS |
Stracke R, Favory JJ, Gruber H, Bartelniewoehner L, Bartels S, Binkert M, Funk M, Weisshaar B, Ulm R (2010a) The Arabidopsis bZIP transcription factor HY5 regulates expression of the PFG1/MYB12 gene in response to light and ultraviolet-B radiation. Plant, Cell & Environment 33, 88–103.
Stracke R, Jahns O, Keck M, Tohge T, Niehaus K, Fernie AR, Weisshaar B (2010b) Analysis of PRODUCTION OF FLAVONOL GLYCOSIDES-dependent flavonol glycoside accumulation in Arabidopsis thaliana plants reveals MYB11-, MYB12- and MYB111-independent flavonol glycoside accumulation. New Phytologist 188, 985–1000.
| Analysis of PRODUCTION OF FLAVONOL GLYCOSIDES-dependent flavonol glycoside accumulation in Arabidopsis thaliana plants reveals MYB11-, MYB12- and MYB111-independent flavonol glycoside accumulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhs1arsL7J&md5=c002a5cbec5bf52cb98bda58de7771d4CAS |
Taylor LP, Grotewold E (2005) Flavonoids as developmental regulators. Current Opinion in Plant Biology 8, 317–323.
| Flavonoids as developmental regulators.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjslKntrs%3D&md5=e0b49068063103d2fc97c7dee6096704CAS |
Treutter D (2005) Significance of flavonoids in plant resistance and enhancement of their biosynthesis. Plant Biology 7, 581–591.
| Significance of flavonoids in plant resistance and enhancement of their biosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xps1eisg%3D%3D&md5=55dbaea2df5e4d19dca81f3e546d8ea9CAS |
Turner LB (1990) Water relations of white clover (Trifolium repens) – water potential gradients and plant morphology. Annals of Botany 65, 285–290.
Turner LB (1991) The effect of water-stress on the vegetative growth of white clover (Trifolium repens L) – comparison of long-term water deficit and a short-term developing water-stress. Journal of Experimental Botany 42, 311–316.
| The effect of water-stress on the vegetative growth of white clover (Trifolium repens L) – comparison of long-term water deficit and a short-term developing water-stress.Crossref | GoogleScholarGoogle Scholar |
Turtola S, Rousi M, Pusenius J, Yamaji K, Heiska S, Tirkkonen V, Meier B, Julkunen-Tiitto R (2005) Clone-specific responses in leaf phenolics of willows exposed to enhanced UV-B radiation and drought stress. Global Change Biology 11, 1655–1663.
| Clone-specific responses in leaf phenolics of willows exposed to enhanced UV-B radiation and drought stress.Crossref | GoogleScholarGoogle Scholar |
Virk DS, Pandit DB, Sufian MA, Ahmed F, Siddique MAB, Samad MA, Rahman MM, Islam MM, Ortiz-Ferrara G, Joshi KD, Witcombe JR (2009) REML is an effective analysis for mixed modelling of unbalanced on-farm varietal trials. Experimental Agriculture 45, 77–91.
| REML is an effective analysis for mixed modelling of unbalanced on-farm varietal trials.Crossref | GoogleScholarGoogle Scholar |
Ward AD (1963) Hierarchical grouping to optimise an objective function. Journal of the American Statistical Association 58, 236–244.
| Hierarchical grouping to optimise an objective function.Crossref | GoogleScholarGoogle Scholar |
Watson SL, DeLacy IH, Podlich DW, Basford KE (1995) GEBEIL: an analysis package using agglomerative hierarchical classificatory and SVD ordination procedures for genotype × environment data. (Centre for Statistics Research Report: Brisbane)
Winkel BSJ (2006) The biosynthesis of flavonoids. In ‘The science of flavonoids.’ (Ed. E Grotewold) pp. 71–95. (Springer: New York)
Winkel-Shirley B (2002) Biosynthesis of flavonoids and effects of stress. Current Opinion in Plant Biology 5, 218–223.
| Biosynthesis of flavonoids and effects of stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XivVSmurg%3D&md5=774120c92fd8c8ce9c657bf34d10f77eCAS |
Wishart D (1969) Algorithm for hierarchical classifications. Biometrics 25, 165–170.
| Algorithm for hierarchical classifications.Crossref | GoogleScholarGoogle Scholar |
Woodfield DR, Clifford PTP, Cousins GR, Ford JL, Baird IJ, Miller JE, Woodward SL, Caradus JR (2001) Grasslands Kopu II and Crusader: new generation white clovers. Proceedings of the New Zealand Grassland Association 63, 103–108.
Yamasaki H, Sakihama Y, Ikehara N (1997) Flavonoid-peroxidase reaction as a detoxification mechanism of plant cells against H2O2. Plant Physiology 115, 1405–1412.
Yang W-J, Wu Y-M, Tang Y-X (2009) Expressing and functional analysis of GmMYBJ6 from soybean. Yi Chuan 31, 645–653.
| Expressing and functional analysis of GmMYBJ6 from soybean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1agu7jP&md5=ab9b3ad9760f875af269d60610880077CAS |