Induction of Synthetic Polyploids and Assessment of Genomic Stability in Lippia alba

Frontiers in Plant Science

Volumn 11, Issue , 2020, Pages

  Julião, Sirlei Aparecida ^a   Ribeiro, Christiane do Valle ^a   Lopes, Juliana Mainenti Leal ^a   Matos, Elyabe Monteiro de ^a   Reis, Aryane Campos ^a   Peixoto, Paulo Henrique Pereira ^a   Machado, Marco Antonio ^b   Azevedo, Ana Luisa Sousa ^b   Grazul, Richard Michael ^a   Campos, José Marcello Salabert de ^a   Viccini, Lyderson Facio ^a  

^a FEDERAL UNIVERSITY OF JUIZ DE FORA   (Brazil)

^b EMBRAPA CERRADOS   (Brazil)

Author keywords

artificial polyploidy; colchicine; essential oil; FISH; flow cytometry; genomic instability; medicinal plants; SSR and ISSR markers

Indexed keywords

EID: 85083105986     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2020.00292     Document Type: Article

References (95)

1. Adams K. L., Wendel J. F., (2005). Polyploidy and genome evolution in plants. Curr. Opin. Plant Biol. 8 135–141. 10.1016/j.pbi.2005.01.001 15752992
2. Adams R. P., (2007). Identification of Essential Oil Components by Gas Chromatography/Mass Spectrometry 4 Edn. Carol Stream, IL: Allured.
3. Albert V. A., Barbazuk W. B., de Pamphilis C. W., Der J. P., Leebens-Mack J., Ma H., et al. (2013). The Amborella genome and the evolution of flowering plants. Science 342:1241089. 10.1126/science.1241089 24357323
4. Allario T., Brumos J., Colmenero-Flores J. M., Tadeo F., Froelicher Y., Talon M., et al. (2011). Large changes in anatomy and physiology between diploid Rangpur lime (Citrus limonia) and its autotetraploid are not associated with large changes in leaf gene expression. J. Exp. Bot. 62 2507–2519. 10.1093/jxb/erq467 21273338
5. Allum J. F., Bringloe D. H., Roberts A. V., (2007). Chromosome doubling in a Rosa rugosa Thunb. hybrid by exposure of in vitro nodes to oryzalin: the effects of node length, oryzalin concentration and exposure time. Plant Cell Rep. 26 1977–1984. 17641861
6. Aversano R., Caruso I., Aronne G., De Micco V., Scognamiglio N., Carputo D., (2013). Stochastic changes affect Solanum wild species following autopolyploidization. J. Exp. Bot. 64 625–635. 10.1093/jxb/ers357 23307917
7. Aversano R., Ercolano M. R., Caruso I., Fasano C., Rosellini D., Carputo D., (2012). Molecular tools for exploring polyploid genomes in plants. Int. J. Mol. 13 10316–10335. 10.3390/ijms130810316 22949863
8. Aversano R., Scarano M. T., Aronne G., Caruso I., D’amelia V., De Micco V., et al. (2015). Genotype-specific changes associated to early synthesis of autotetraploids in wild potato species. Euphytica 202 307–316. 10.1007/s10681-014-1338-3
9. Blasco M., Badenes M. L., Naval M. M., (2015). Colchicine-induced polyploidy in loquat (Eriobotrya japonica (Thunb.) (Lindl.). Plant Cell Tissue Organ Cult. 2 453–461. 10.1007/s11240-014-0612-3
10. Buggs R. J., Soltis P. S., Mavrodiev E. V., Symonds V. V., Soltis D. E., (2008). Does phylogenetic distance between parental genomes govern the success of polyploids. Castanea 73 74–93. 10.2179/0008-7475(2008)73[74:dpdbpg]2.0.co;2
11. Campos J. M. S., Sousa S. M., Silva P. S., Pinheiro L. C., Sampaio F., Viccini L. F., (2011). Chromosome numbers and DNA C values in the genus Lippia (Verbenaceae). Plant Syst. Evol. 291 133–140. 10.1007/s00606-010-0370-6
12. Caruso I., Lepore L., De Tommasi N., Dal Piaz F., Frusciante L., Aversano R., et al. (2011). Secondary Metabolite profile in induced tetraploids of wild Solanum commersonii, Dun. Chem. Biodivers. 8 2226–2237. 10.1002/cbdv.201100038 22162160
13. Carvalho C. R., Saraiva L. S., (1993). A new heterochromatin banding pattern revealed by modified HKG banding technique for maize chromosomes. Heredity 70 515–519. 10.1038/hdy.1993.74
14. Castro M., Castro S., Loureiro J., (2018). Production of synthetic tetraploids as a tool for polyploid research. Web Ecol. 18 129–141. 10.5194/we-18-129-2018
15. Chies C. E., Branco C. S., Scola G., Agostini F., Gower A. E., Salvador M., (2013). Antioxidant effect of Lippia alba (Miller) NE Brown. Antioxidants 2 194–205. 10.3390/antiox2040194 26784458
16. Chung H., Shi H., Huang B., Chen J., (2017). Enhanced agronomic traits and medicinal constituents of autotetraploids in Anoectochilus formosanus Hayata, a top-grade medicinal orchid. Molecules 22 1–13. 10.3390/molecules22111907 29112129
17. Cui Y., Hou L., Li X., Huang F., Pang X., Li Y., (2017). In vitro induction of tetraploid Ziziphus jujuba Mill. var. spinosa plants from leaf explants. Plant Cell Tissue Organ Cult. 131 175–182.
18. Dehghan E., Häkkinen S. T., Oksman-Caldentey K. M., Ahmadi F. S., (2012). Production of tropane alkaloids in diploid and tetraploid plants and in vitro hairy root cultures of Egyptian henbane (Hyoscyamus muticus L.). Plant Cell Tissue Organ Cult. 110 35–44. 10.1007/s11240-012-0127-8
19. Denaeghe H. E. R., Van Laere K., Leus L., Lootens P., Van Huylenbroeck J., Van Labeke M.-C., (2018). The Variable Effect of Polyploidization on the Phenotype in Escallonia. Front. Plant Sci. 9:354. 10.3389/fpls.2018.00354 29616065
20. Dhooghe E., Van Laere K., Eeckhaut T., Leus L., Van Huylenbroeck J., (2011). Mitotic chromosome doubling of plant tissues in vitro. Plant Cell Tissue Organ Cult. 104 359–373. 10.1007/s11240-010-9786-5
21. Dodsworth S., Chase M. W., Leitch A. R., (2016). Is post-polyploidization diploidization the key to the evolutionary success of angiosperms? Bot. J. Linn. Soc. 180 1–5. 10.1111/boj.12357
22. Dolezel J., Greilhuber J., Suda J., (2007). Estimation of nuclear DNA content in plants using flow cytometry. Nat. Protoc. 2 2233–2244. 10.1038/nprot.2007.310 17853881
23. Doyle J. J., Coate J. E., (2019). Polyploidy, the nucleotype, and novelty: the impact of genome doubling on the biology of the cell. Int. J. Plant Sci. 180 1–52. 10.1086/700636
24. Doyle J. J., Doyle J. L., (1990). Isolation of plant DNA from fresh tissue. Focus 12 13–15.
25. Earl D. A., VonHoldt B. M., (2012). STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv. Genet. Resour. 4 359–361. 10.1007/s12686-011-9548-7
26. Eng W.-H., Ho W.-S., (2019). Polyploidization using colchicine in horticultural plants: a review. Sci. Hortic. 246 604–617. 10.1016/j.scienta.2018.11.010
27. Evanno G., Regnaut S., Goudet J., (2005). Detecting the number of clusters of individuals using the software structure: a simulation study. Mol. Ecol. 14 2611–2620. 10.1111/j.1365-294x.2005.02553.x 15969739
28. Ewald D., Ulrich K., Naujoks G., Schröder M. B., (2009). Induction of tetraploid poplar and black locust plants using colchicine: chloroplast number as an early marker for selecting polyploids in vitro. Plant Cell Tissue Organ Cult. 99 353–357. 10.1007/s11240-009-9601-3
29. Fasano C., Diretto G., Aversano R., D’agostino N., Di Matteo A., Frusciante L., et al. (2016). Transcriptome and metabolome of synthetic Solanum autotetraploids reveal key genomic stress events following polyploidization. New Phytol. 210 1382–1394. 10.1111/nph.13878 26915816
30. Galbraith D. W., Harkins K. R., Maddon J. M., Ayres N. M., Sharma D. P., Firoozabady E., (1983). Rapid flow cytometric analysis of the cell-cycle in intact plant-tissues. Science 220 1049–1051. 10.1126/science.220.4601.1049 17754551
31. Gao R., Wang H., Dong B., Yang X., Chen S., Jiang J., et al. (2016). Morphological, genome and gene expression changes in newly induced autopolyploid Chrysanthemum lavandulifolium (Fisch. ex Trautv.) Makino. Int. J. Mol. 17:1690. 10.3390/ijms17101690 27735845
32. Glamočlija J., Soković M., Tešević V., Linde G. A., Colauto N., (2011). Chemical characterization of Lippia alba essential oil: an alternative to control green molds. Braz. J. Microbiol. 42 1537–1546. 10.1590/S1517-83822011000400041 24031788
33. Gomes S. S. L., Saldanha C. W., Neves C. S., Trevizani M., Raposo N. R. B., Notini M. M., et al. (2014). Karyotype, genome size, and in vitro chromosome doubling of Pfaffia glomerata (Spreng.) Pedersen. Plant Cell Tissue Organ Cult. 118 45–56.
34. Grant V., (1981). Plant Speciation 2nd Edn. New York, NY: Columbia University Press.
35. Hammer Ø., Harper D. A., Ryan P. D., (2001). PAST: paleontological statistics software package for education and data analysis. Palaeontol. Electron. 4 1–9.
36. Hannweg K., Visser G., de Jager K., Bertling I., (2016). In vitro-induced polyploidy and its effect on horticultural characteristics, essential oil composition and bioactivity of Tetradenia riparia. S. Afr. J. Bot. 106 186–191. 10.1016/j.sajb.2016.07.013
37. Harbard J. L., Griffin A. R., Foster S., Brooker C., Kha L. D., Koutoulis A., (2012). Production of colchicine-induced autotetraploids as a basis for sterility breeding in Acacia mangium Willd. Forestry 85 427–436. 10.1093/forestry/cps041
38. Hegarty M., Coate J., Sherman-Broyles S., Abbott R., Hiscock S., Doyle J., (2013). Lessons from natural and artificial polyploids in higher plants. Cytogenet. Genome Res. 140 204–225. 10.1159/000353361 23816545
39. Hennebelle T., Sahpaz S., Joseph H., Bailleul F., (2008). Ethnopharmacology of Lippia alba. J. Ethnopharmacol. 116 211–222. 10.1016/j.jep.2007.11.044 18207682
40. Iannicelli J., Elechosa M. A., Juárez M. A., Martínez A., Bugallo V., Bandoni A. L., et al. (2016). Effect of polyploidization in the production of essential oils in Lippia integrifolia. Ind. Crop. Prod. 81 20–29. 10.1016/j.indcrop.2015.11.053
41. Iannicelli J., Guariniello J., Tossi V. E., Regalado J. J., Di Ciaccio L., Van Baren C. M., et al. (2020). The “polyploid effect” in the breeding of aromatic and medicinal species. Sci. Hortic. 260:108854. 10.1016/j.scienta.2019.108854 28797221
42. Jezler C. N., De Oliveira A. R., Batista R. S., Oliveira R. A., Silva D. D. C., Costa L. C. D. B., (2013). Lippia alba morphotypes cidreira and melissa exhibit significant differences in leaf characteristics and essential oil profile. Rev. Bras. Farmacogn. 23 217–223.
43. Jiang J., Gill B. S., Wang G.-L., Ronald P. C., Ward D. C., (1995). Metaphase and interphase fluorescence in situ hybridization mapping of the rice genome with bacterial artificial chromosomes. Proc. Natl. Acad. Sci. U.S.A. 92 4487–4491. 10.1073/pnas.92.10.4487 7753830
44. Jiao Y., Wickett N. J., Ayyampalayam S., Chanderbali A. S., Landherr L., Ralph P. E., et al. (2011). Ancestral polyploidy in seed plants and angiosperms. Nature 473 97–100. 10.1038/nature09916 21478875
45. Lehrer J., Brand M., Lubell J., (2008). Induction of tetraploidy in meristematically active seeds of Japanese barberry (Berberis thunbergii var. atropurpurea) through exposure to colchicine and oryzalin. Sci. Hort. 119 67–71. 10.1016/j.scienta.2008.07.003
46. Long Y. L., Qiao F., Jiang X. F., Cong H. Q., Sun M. L., Xu Z. J., (2019). Screening and analysis on the differentially expression genes between diploid and autotetraploid watermelon by using of digital gene expression profile. Braz. J. Biol. 79 180–190. 10.1590/1519-6984.174475 29924132
47. Lopes J. M. L., Carvalho H. H., Zorzatto C., Azevedo A. L., Machado M. A., Salimena F. R. G., et al. (2019). Genetic relationships and polyploid origins in the Lippia alba complex. Am. J. Bot. 107 1–11.
48. Manica-Cattani M. F., Zacaria J., Pauletti G., Atti-Serafini L., Cheverrigaray S., (2009). Genetic variation among South Brazilian accessions of Lippia alba Mill. (Verbenaceae) detected by ISSR and RAPD markers. Braz. J. Biol. 69 375–380. 10.1590/s1519-69842009000200020 19675941
49. Marchant D. B., Soltis D. E., Soltis P. S., (2016). Patterns of abiotic niche shifts in allopolyploids relative to their progenitors. New Phytol. 212 708–718. 10.1111/nph.14069 27399976
50. Martelotto L. G., Ortiz J. P. A., Stein J., Espinoza F., Quarin C. L., Pessino S. C., (2007). Genome rearrangements derived from autopolyploidization in Paspalum sp. Plant Sci. 172 970–977. 10.1016/j.plantsci.2007.02.001
51. Mecchia M. A., Ochogavía A., Selva J. P., Laspina N., Felitti S., Martelotto L. G., et al. (2007). Genome polymorphisms and gene differential expression in a ‘back-and-forth’ ploidy-altered series of weeping lovegrass (Eragrostis curvula). J. Plant Physiol. 164 1051–1061. 10.1016/j.jplph.2006.07.002 16919366
52. Münzbergová Z., (2017). Colchicine application significantly affects plant performance in the second generation of synthetic polyploids and its effects vary between populations. Ann. Bot. 120 329–339. 10.1093/aob/mcx070 28633349
53. Nebel B. R., (1937). Mechanism of Polyploidy through Colchicine. Nature 14:1101. 10.1038/1401101a0
54. Niel E., Scherrmann J. M., (2006). Colchicine today. Joint Bone Spine 73 673–678. 10.1016/j.jbspin.2006.03.006 17067838
55. Otto S. P., Whitton J., (2000). Polyploid incidence and evolution. Annu. Rev. Genet. 34 401–437. 10.1146/annurev.genet.34.1.401 11092833
56. Pavlíková Z., Paštová L., Münzbergová Z., (2017). Synthetic polyploids in Vicia cracca: methodology, effects on plant performance and aneuploidy. Plant Syst. Evol. 303 827–839. 10.1007/s00606-017-1414-y
57. Peixoto M. G., Costa-Júnior L. M., Blank A. F., Da Silva Lima A., Menezes T. S. A., De Alexandria Santos D., et al. (2015). Acaricidal activity of essential oils from Lippia alba genotypes and its major components carvone, limonene, and citral against Rhipicephalus microplus. Vet. Parasitol. 210 118–122. 10.1016/j.vetpar.2015.03.010 25837783
58. Pierre P. M., Sousa S. M., Davide L. C., Machado M. A., Viccini L. F., (2011). Karyotype analysis, DNA content and molecular screening in Lippia alba (Verbenaceae). An. Acad. Bras. Cien. 83 993–1006. 10.1590/s0001-37652011005000012 21739084
59. Pritchard J. K., Stephens M., Donnelly P., (2000). Inference of population structure using multilocus genotype data. Genetics 155 945–959. 10835412
60. Ramasamy R. K., Ramasamy S., Bindroo B. B., Naik V. G., (2014). Structure plot: a program for drawing elegant structure bar plots in user friendly interface. Springerplus 3:431. 10.1186/2193-1801-3-431 25152854
61. Ramsey J. R., Schemske D. W., (2002). Neopolyploidy in flowering plants. Annu. Rev. Ecol. Syst. 33 589–639. 10.1146/annurev.ecolsys.33.010802.150437
62. Regalado J. J., Carmona-Martín E., Querol V., Veléz C. G., Encina C. L., Pitta-Alvarez S. I., (2017). Production of compact petunias through polyploidization. Plant Cell Tissue Organ Cult. 129 61–71. 10.1007/s11240-016-1156-5
63. Rêgo M. D., Rêgo E. R., Bruckner C. H., Finger F. L., Otoni W. C., (2011). In vitro induction of autotetraploids from diploid yellow passion fruit mediated by colchicine and oryzalin. Plant Cell Tissue Organ Cult. 107 451–459. 10.1007/s11240-011-9995-6
64. Reis A. C., Sousa S. M., Vale A. A., Pierre P. M. O., Franco A. L., Campos J. M. S., et al. (2014). Lippia alba (Mill.) N. E. Br. (Verbenaceae): a new tropical autopolyploid complex? Am. J. Bot. 101 1002–1012. 24920764
65. Rice A., Šmarda P., Novosolov M., Drori M., Glick L., Sabath N., et al. (2019). The global biogeography of polyploid plants. Nat. Ecol. Evol. 3 265–273. 10.1038/s41559-018-0787-9 30697006
66. Rohlf F. J., (2000). NTSYS-Pc Numerical Taxonomy and Multivariate Analysis System, version 2.1. New York, NY: Exeter Publishing Setauket.
67. Sadat-Noori A. S., Maryam N., Ghasem K., Shirkool K. H., Mohsen N., (2017). Effect of colchicine-induced polyploidy on morphological characteristics and essential oil composition of ajowan (Trachyspermum ammi L.). Plant Cell Tissue Organ Cult. 130 543–551. 10.1007/s11240-017-1245-0
68. Sajjad A., Jaskani M., Mehmood A., Ahmad I., (2013). Effect of colchicine on in vitro polyploidy induction in African marigold (Tagetes erecta). Pak. J. Bot. 45 1255–1258.
69. Salma U., Kundu S., Mandal N., (2017). Artificial polyploidy in medicinal plants: advancement in the last two decades and impending prospects. J. Crop. Sci. Biotechnol. 20 9–19. 10.1007/s12892-016-0080-1
70. Sattler M. C., Carvalho C. R., Clarindo W. R., (2016). The polyploidy and its key role in plant breeding. Planta 243 281–296. 10.1007/s00425-015-2450-x 26715561
71. Soltis D. E., Soltis P. S., Bennett M. D., Leitch I. J., (2003). Evolution of genome size in the angiosperms. Am. J. Bot. 90 1596–1603. 10.3732/ajb.90.11.1596 21653334
72. Soltis P. S., Soltis D. E., (2009). The role of hybridization in plant speciation. Annu. Rev. Plant Biol. 60 561–588. 10.1146/annurev.arplant.043008.092039 19575590
73. Soltis P. S., Soltis D. E., (2012). Polyploidy and Genome Evolution. Berlin: Springer.
74. Stebbins G. L., (1971). Chromosomal Evolution in Higher Plants. London: Edward Arnold.
75. Stift M., Koláø F., Meirmans P. G., (2019). STRUCTURE is more robust than other clustering methods in simulated mixed-ploidy populations. Heredity 123 429–441. 10.1038/s41437-019-0247-6 31285566
76. Sun Q., Sun H., Li L., Bell R. L., (2009). In vitro colchicine-induced polyploid plantlet production and regeneration from leaf explants of the diploid pear (Pyrus communis L.) cultivar, ‘Fertility’. J. Hortic. Sci. Biotechnol. 84 548–552. 10.1080/14620316.2009.11512564
77. Tavan M., Mirjalili M. H., Karimzadeh G., (2015). In vitro polyploidy induction: changes in morphological, anatomical and phytochemical characteristics of Thymus persicus (Lamiaceae). Plant Cell Tissue Organ Cult. 122 573–583. 10.1007/s11240-015-0789-0
78. Tayalé A., Parisod C., (2013). Natural pathways to polyploidy in plants and consequences for genome reorganization. Cytogenet. Genome Res. 140 79–96. 10.1159/000351318 23751271
79. Trojak-Goluch A., Skomra U., (2013). Artificially induced polyploidization in Humulus lupulus L. and its effect on morphological and chemical traits. Breed. Sci. 63 393–399. 10.1270/jsbbs.63.393 24399911
80. Väinölä A., (2000). Polyploidization and early screening of Rhododendron hybrids. Euphytica 112 239–244.
81. Van de Peer Y., Mizrachi E., Marchal K., (2017). The evolutionary significance of polyploidy. Nat. Rev. Genet. 18 411–424. 10.1038/nrg.2017.26 28502977
82. Vanstechelman I., Eeckhaut T., Van Huylenbroeck J., Van Labeke M. C., (2010). Histogenic analysis of chemically induced mixoploids in Spathiphyllum wallisii. Euphytica 174 61–72. 10.1007/s10681-010-0133-z
83. Viccini L. F., Pierre P. M. O., Praça M. M., Da Costa D. S., Romanel E. C., Sousa S. M., et al. (2005). Chromosome numbers in the genus Lippia (Verbenaceae). Plant Syst. Evol. 256 171–178. 10.1007/s00606-005-0351-3 23460443
84. Viccini L. F., Silveira R. S., Vale A. A., Campos J. M. S., Reis A. C., Santos M. O., et al. (2014). Citral and linalool content has been correlated to DNA content in Lippia alba (Mill.) NE Brown (Verbenaceae). Ind. Crop. Prod. 59 14–19. 10.1016/j.indcrop.2014.04.028
85. Vieira D. D. S. S., Emiliani G., Michelozzid M., Centritto M., Luro F., Morillonf R., et al. (2016). Polyploidization alters constitutive content of volatile organic compounds (VOC) and improves membrane stability under water deficit in Volkamer lemon (Citrus limonia Osb.) leaves. Environ. Exp. Bot. 126 1–9. 10.1016/j.envexpbot.2016.02.010
86. Wang C. G., Li H., Xue Z. Y., Chen C. B., Gu Y., Sun D. L., et al. (2009). Marker-based analysis of genome structure and DNA methylation in a watermelon (Citrullus lanatus) ploidy series. Bot. Stud. 50 389–402.
87. Wei K. H., Xu J. P., Li L. X., Cai J. Y., Miao J. H., Li M. H., (2018). In vitro induction and generation of tetraploid plants of Sophora tonkinensis Gapnep. Pharmacogn. Mag. 14 149–154. 10.4103/pm.pm_170_17 29720823
88. Wendel J. F., (2015). The wondrous cycles of polyploidy in plants. Am. J. Bot. 102 1753–1756. 10.3732/ajb.1500320 26451037
89. Wendel J. F., Jackson S. A., Meyers B. C., Wing R. A., (2016). Evolution of plant genome architecture. Genome Biol. 17 1–14.
90. Widoretno W., (2016). In vitro induction and characterization of tetraploid Patchouli (Pogostemon cablin Benth.) plant. Plant Cell Tissue Organ Cult. 125 261–267.
91. Xu C. G., Tang T. X., Chen R., Liang C. H., Liu X. Y., Wu C. L., et al. (2014). A comparative study of bioactive secondary metabolite production in diploid and tetraploid Echinacea purpurea (L.) Moench. Plant Cell Tissue Organ Cult. 116 323–332. 10.1007/s11240-013-0406-z
92. Yan H. J., Xiong Y., Zhang H. Y., He M. L., (2016). In vitro induction and morphological characteristics of octoploid plants in Pogostemon cablin. Breeding Sci. 66 169–174. 10.1270/jsbbs.66.169 27162488
93. Yang H. L., Liu J., Huang S. M., Guo T. T., Deng L. B., Hua W., (2014). Selection and evaluation of novel reference genes for quantitative reverse transcription PCR (qRT-PCR) based on genome and transcriptome data in Brassica napus L. Gene 538 113–122. 10.1016/j.gene.2013.12.057 24406618
94. Zhou H., Zeng W., Yan H., (2017). In vitro induction of tetraploids in cassava variety ‘Xinxuan 048’ using colchicine. Plant Cell Tissue Organ Cult. 128 723–729. 10.1007/s13258-018-0692-2 30155710
95. Zlesak D. C., Thill C. A., Anderson N. O., (2005). Trifluralin-mediated polyploidization of Rosa chinensis minima (Sims) Voss seedlings. Euphytica 141 281–290. 10.1007/s10681-005-7512-x