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Long distance pollen-mediated flow of herbicide resistance genes in Lolium rigidum

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Abstract

Gene flow promotes genetic exchange among plant populations mediating evolutionary dynamics; yet, the importance of gene flow at distance via pollen movement is poorly understood. A field experiment at the landscape level was conducted with Lolium rigidum herbicide-susceptible individuals (population VLR1) placed into an otherwise Lolium-free bushland environment at increasing distances from adjacent large commercial crop fields infested with herbicide-resistant L. rigidum. Herbicide resistance was used as a marker to quantify the distance and the rate of pollen-mediated gene flow. About 21,245 seeds were produced on the isolated, susceptible mother plants of which 3,303 seedlings were tested for herbicide resistance and 664 seedlings were found to be resistant. Pollen-mediated gene flow occurred at 3,000 m (maximum tested distance). Both Mendelian and molecular analyses (sequencing and CAPS markers) confirmed the introgression of herbicide resistance genes. This is the first documented case of long-distance gene flow in L. rigidum. The results are important for future modeling simulations of herbicide resistance evolution and subsequent mobility. The adoption of integrated agronomic strategies, the control of potential receptor plants on fields’ margins and conservative use of herbicides can be realistic options to minimize herbicide resistance spread.

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References

  • Ahloowalia BS (1973) Germination in vitro of ryegrass pollen grains. Euphytica 22:575–581

    Article  Google Scholar 

  • Baker J, Preston C (2006) Preliminary investigations of the effects of pollen competition on gene flow in the wind pollinated species annual ryegrass (Lolium rigidum Gaud.) 15th Australian Weeds Conference, 24–28 September 2006. Adelaide Conference Centre, Adelaide, South Australia p 543

  • Balfourier F, Imbert C, Charmet G (2000) Evidence for phylogeographic structure in Lolium species related to the spread of agriculture in Europe. A cpDNA study. Theor Appl Genet 101:131–138

    Article  CAS  Google Scholar 

  • Borger CPD, Walsh M, Scott JK, Powles SB (2007) Tumbleweeds in the Western Australian cropping system: seed dispersal characteristics of Salsola australis. Weed Res 47:406–414

    Article  Google Scholar 

  • Christopher JT, Powles SB, Holtum JAM (1992) Resistance to acetolactate synthase-inhibiting herbicides in annual ryegrass (Lolium rigidum) involves at least two mechanisms. Plant Physiol 100:1909–1913

    Article  PubMed  CAS  Google Scholar 

  • Cunliffe KV, Vecchies AC, Jones ES, Kearney GA, Forster JW, Spangenberg GC, Smith KF (2004) Assessment of gene flow using tetraploid genotypes of perennial ryegrass (Lolium perenne L.). Aust J Agric Res 55:389–396

    Article  CAS  Google Scholar 

  • Darmency H (1996) Movement of resistance genes among plants. In: Brown TM (ed) Molecular genetics and evolution of pesticide resistance in plants: biology and biochemistry. Lewis Publishers, Boca Raton, pp 209–220

    Google Scholar 

  • Dauer JT, Mortensen DA, Vangessel MJ (2007) Temporal and spatial dynamics of long-distance Conyza canadensis seed dispersal. J Appl Ecol 44:105–114

    Article  Google Scholar 

  • Devaux C, Lavigne C, Falentin-Guyomarch H, Vautrin S, Lecomte J, Klein EK (2005) High diversity of oilseed rape pollen clouds over an agro-ecosystem indicates long-distance dispersal. Mol Ecol 14:2269–2280

    Article  PubMed  CAS  Google Scholar 

  • Diggle AJ, Neve P (2001) The population dynamics and genetics of herbicide resistance—a modelling approach. In: Powles SB, Shaner DL (eds) Herbicide resistance and world grains. CRC Press, Baton Rouge, pp 61–99

    Google Scholar 

  • Diggle AJ, Neve PB, Smith FP (2003) Herbicides used in combination can reduce the probability of herbicide resistance in finite weed populations. Weed Res 43:371–382

    Article  Google Scholar 

  • Ehrlich PR, Raven PH (1969) Differentiation in populations. Science 165:1228–1232

    Article  PubMed  CAS  Google Scholar 

  • Fei S, Nelson E (2003) Estimation of pollen viability, shedding pattern, and longevity of creeping bentgrass on artificial media. Crop Sci 43:2177–2181

    Google Scholar 

  • Gaines TA, Byrne PF, Westra P, Nissen SJ, Brien Henry WDLS, Chapman PL (2007) An empirically derived model of field-scale gene flow in winter wheat. Crop Sci 47:2308–2316

    Article  Google Scholar 

  • Ghersa CM, Martinezghersa MA, Brewer TG, Roush ML (1994) Use of gene flow to control diclofop-methyl resistance in Italian ryegrass (Lolium multiflorum). Weed Technol 8:139–147

    CAS  Google Scholar 

  • Giddings GD (2000) Modelling the spread of pollen from Lolium perenne. The implications for the release of wind-pollinated transgenics. Theor Appl Genet 100:971–974

    Article  Google Scholar 

  • Giddings GD, Sackville Hamilton NR, Hayward MD (1997) The release of genetically modified grasses. Part 1: pollen dispersal to traps in Lolium perenne. Theor Appl Genet 94:1000–1006

    Article  Google Scholar 

  • Gill GS (1996) Why annual ryegrass is a problem in Australian agriculture. Plant Prot Q 11:193–195

    Google Scholar 

  • Goggi SA, Lopez-Sanchez H, Caragea P, Westgate M, Raymond A, Clark CA (2007) Gene flow in maize fields with different local pollen densities. Int J Biometeorol 51:493–503

    Article  PubMed  Google Scholar 

  • Jaseniuk M, Brulé-Babel AL, Morrison IN (1996) The evolution and genetics of herbicide resistance in weeds. Weed Sci 44:176–193

    Google Scholar 

  • Levin DA, Kerster HW (1974) Gene flow in seed plants. Evol Biol 7:139–220

    Google Scholar 

  • Llewellyn RS, Allen DB (2006) Expected mobility of herbicide resistance via weed seeds and pollen in a Western Australian cropping region. Crop Prot 25:520–526

    Article  CAS  Google Scholar 

  • Lu YQ, Baker J, Preston C (2007) The spread of resistance to acetolactate synthase inhibiting herbicides in a wind-borne, self-pollinated weed species, Lactuca serriola L. Theor Appl Genet 115:443–450

    Article  PubMed  CAS  Google Scholar 

  • Luna SV, Figueroa JM, Baltazar BM, Gomez RL, Townsend R, Shchoper JB (2001) Maize pollen longevity and distance isolation requirements for effective pollen control. Crop Sci 41:1551–1557

    Google Scholar 

  • McCraw LM, Spoor W (1983) Self-incompatibility in Lolium species. 1. Lolium rigidum Gaud. and L. multiflorum L. Heredity 1:21–27

    Article  Google Scholar 

  • Messeguer J, Marfa V, Catala MM, Guiderdoni E, Mele E (2004) A field study of pollen-mediated gene flow from Mediterranean GM rice to conventional rice and the red rice weed. Mol Breed 13:103–112

    Article  CAS  Google Scholar 

  • Murray BG, Morrison IN, Friesen LF (2002) Pollen-mediated gene flow in wild oat. Weed Sci 50:321–325

    Article  CAS  Google Scholar 

  • Nurminiemi M, Tufto J, Nilsson N-O, Rognli OA (1998) Spatial models of pollen dispersal in the forage grass meadow fescue. Evol Ecol 12:487–502

    Article  Google Scholar 

  • Owen MC, Walsh MJ, Llewellyn RS, Powles SB (2007) Widespread evolution of multiple herbicide resistance in annual ryegrass (Lolium rigidum) populations within the Western Australian wheat belt. Aust J Agric Res 58:711–718

    Article  CAS  Google Scholar 

  • Pfender W, Graw R, Bradley W, Carney M, Maxwell L (2007) Emission rates, survival, and modeled dispersal of viable pollen of creeping bentgrass. Crop Sci 47:2529–2539

    Article  Google Scholar 

  • Rieger MA, Lamond M, Preston C, Powles SB, Roush RT (2002) Pollen-mediated movement of herbicide resistance between commercial canola fields. Science 296:2386–2388

    Article  PubMed  CAS  Google Scholar 

  • Rognli OA, Nilsson N-O, Nurminiemi M (2000) Effects of distance and pollen competition on gene flow in the wind-pollinated Festuca pratensis Huds. Heredity 85:550–560

    Article  PubMed  CAS  Google Scholar 

  • Rong J, Liu B-R, Song Z, Su J, Snow AA, Zhang X, Sun S, Chen R, Wang F (2007) Dramatic reduction of crop-to-crop gene flow within a short distance from transgenic rice fields. New Phytol 173:346–353

    Article  PubMed  Google Scholar 

  • Roux F, Paris M, Reboud X (2008) Delaying weed adaptation to herbicide environmental heterogeneity: a simulation approach. Pest Manag Sci 64:16–29

    Article  PubMed  CAS  Google Scholar 

  • Sokal RR, Rohlf FJ (1969) Biometry. W·H. Freeman and Company, San Francisco

    Google Scholar 

  • Tranel PJ, Wright TR (2002) Resistance of weeds to ALS-inhibiting herbicides: what have we learned? Weed Sci 50:700–712

    Article  CAS  Google Scholar 

  • van Treuren R, Goossens PJ, Sevcikova M (2006) Variation in effective pollination rates in relation to the spatial and temporal distribution of pollen release in rejuvenated perennial ryegrass. Euphytica 147:367–382

    Article  Google Scholar 

  • Wang ZY, Ge Y, Scott M, Spangenberg GC (2004a) Viability and longevity of pollen from transgenic and nontransgenic tall fescue (Festuca arundinacea) (Poaceae) plants. Am J Bot 91:523–530

    Article  Google Scholar 

  • Wang ZY, Lawrence R, Hopkins A, Bell J, Scott M (2004b) Pollen-mediated transgene flow in the wind-pollinated grass species tall fescue (Festuca arundinacea Schreb.). Mol Breed 14:47–60

    Article  Google Scholar 

  • Watrud LS, Lee EH, Fairbrother A, Burdick C, Reichman JR, Bollman M, Storm M, King G, Van de Water PK (2004) Evidence for landscape-level, pollen-mediated gene flow from genetically modified creeping bentgrass with CP4 EPSPS as a marker. Proc Natl Acad Sci 101:14533–14538

    Article  PubMed  CAS  Google Scholar 

  • Weersink A, Llewellynb RS, Pannell DJ (2005) Economics of pre-emptive management to avoid resistance to glyphosate in Australia. Crop Prot 24:659–665

    Article  Google Scholar 

Download references

Acknowledgments

The help of the Guest family is kindly acknowledged. The authors are grateful to Heping Han for assistance in the molecular work. The authors thank Danica Goggin (UWA), Valerie Le Corre (INRA), Christophe Delye (INRA), Pieter Poot (UWA) and Martin Vila-Aiub (UBA-IFEVA) for thoughtful comments on the manuscript. The Western Australian Herbicide Research Initiative (WAHRI) is funded by the Grains Research and Development Corporation of Australia (GRDC).

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Correspondence to Roberto Busi.

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Communicated by J. Snape.

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122_2008_862_MOESM1_ESM.doc

Partial sequencing chromatogram of ALS fragment amplified by primer pair ALS197F/ALS197R and ALS574F/ALS574R from resistant plants of progeny P1. Heterozygosity at the Pro197 codon and the Trp574 codon is arrowed. Y: nucleotide C/T, K: G/T. (DOC 139 kb)

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Busi, R., Yu, Q., Barrett-Lennard, R. et al. Long distance pollen-mediated flow of herbicide resistance genes in Lolium rigidum . Theor Appl Genet 117, 1281–1290 (2008). https://doi.org/10.1007/s00122-008-0862-8

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  • DOI: https://doi.org/10.1007/s00122-008-0862-8

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