Involvement of facultative apomixis in inheritance of EPSPS gene amplification in glyphosate-resistant Amaranthus palmeri

Planta

Volumn 239, Issue 1, 2014, Pages 199-212

  Ribeiro, Daniela N ^a   Pan, Zhiqiang ^b   Duke, Stephen O ^b   Nandula, Vijay K ^c   Baldwin, Brian S ^a   Shaw, David R ^a   Dayan, Franck E ^b  

^a MISSISSIPPI STATE UNIVERSITY   (United States)

^b University   (United States)

^c AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

5 Enolpyruvylshikimate 3 phosphate synthase (EPSPS); Amaranthus palmeri; Apomixis; Asexual reproduction; Facultative apomixis; Glyphosate; Herbicide resistance; Palmer amaranth

Indexed keywords

AMARANTHUS; AMARANTHUS CAUDATUS; AMARANTHUS PALMERI;

3 PHOSPHOSHIKIMATE 1 CARBOXYVINYLTRANSFERASE; DRUG DERIVATIVE; GLYCINE; GLYPHOSATE; HERBICIDE; VEGETABLE PROTEIN;

AMARANTHUS; APOMIXIS; ARTICLE; DRUG EFFECT; DRUG RESISTANCE; GENE AMPLIFICATION; GENE DOSAGE; GENE EXPRESSION REGULATION; GENETIC VARIABILITY; GENETICS; METABOLISM;

3-PHOSPHOSHIKIMATE 1-CARBOXYVINYLTRANSFERASE; AMARANTHUS; APOMIXIS; DRUG RESISTANCE; GENE AMPLIFICATION; GENE DOSAGE; GENE EXPRESSION REGULATION, PLANT; GENETIC VARIATION; GLYCINE; HERBICIDES; PLANT PROTEINS;

EID: 84891629565     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-013-1972-3     Document Type: Article

References (75)

1. Baerson SR, Rodriguez DJ, Tran M, Feng Y, Best NA, Dill GM (2002) Glyphosate-resistant goosegrass: identification of a mutation in the target enzyme 5-enolpyruvylshikimate-3-phosphate synthase. Plant Physiol 129: 1265-1275.
2. Bass C, Field LM (2011) Gene amplification and insecticide resistance. Pest Manag Sci 67: 886-890.
3. Bensch CN, Horak MJ, Peterson D (2003) Interference of redroot pigweed (Amaranthus retroflexus), Palmer amaranth (A. palmeri), and common waterhemp (A. rudis) in soybean. Weed Sci 51: 37-43.
4. Bonny S (2011) Herbicide-tolerant transgenic soybean over 15 years of cultivation: pesticide use, weed resistance, and some economic issues. The case of the USA. Sustainability 3: 1302-1322.
5. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem 72: 248-254.
6. Bradshaw LD, Padgette SR, Kimball SL, Wells BH (1997) Perspectives on glyphosate resistance. Weed Technol 11: 189-198.
7. Brookes G, Barfoot P (2013) The global income and production effects of genetically modified (GM) crops 1996-2011. GM Crops Food 4: 1-10.
8. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55: 611-622.
9. Chan KF, Sun M (1997) Genetic diversity and relationships detected by isozyme and RAPD analysis of crop and wild species of Amaranthus. Theor Appl Genet 95: 865-873.
10. Chandi A, Milla-Lewis SR, Giacomini D, Westra P, Preston C, Jordan DL, York AC, Burton JD, Whitaker JR (2012) Inheritance of evolved glyphosate resistance in a North Carolina Palmer amaranth (Amaranthus palmeri) biotype. Int J Agron. doi: 10. 1155/2012/176108.
11. Chandi A, Jordan DL, Milla-Lewis SR, Jordan DL, York AC, Burton JD, Zuleta CM, Whitaker JR, Culpepper AS (2013) Use of AFLP markers to assess genetic diversity in Palmer amaranth (Amaranthus palmeri) populations from North Carolina and Georgia. Weed Sci 61: 136-145.
12. Chandrika M, Rai VR, Thoyajaksha V (2010) ISSR marker based analysis of micropropagated plantlets of Nothapodytes foetida. Biol Plant 54: 561-565.
13. Chattopadhyay D, Sharma AK (1991) Sex determination in dioecious species of plants. Feddes Repertorium 102: 29-55.
14. Culpepper AS, Grey TL, Vencill WK, Kichler JM, Webster TM, Brown SM, York AC, Davis JW, Hanna WW (2006) Glyphosate-resistant Palmer amaranth (Amaranthus palmeri) confirmed in Georgia. Weed Sci 54: 620-626.
15. Dayan FE, Owens DK, Corniani N, Silva FML, Watson SB, Howell J, Shaner DL (2013) Biochemical markers and enzyme assays for herbicide mode of action and resistance studies. Weed Sci. doi: 10. 1614/WS-D-11-00194. 1.
16. Duke SO, Powles SB (2008) Glyphosate: a once in a century herbicide. Pest Manag Sci 64: 319-325.
17. Duke SO, Powles SB (2009) Glyphosate-resistant crops and weeds: now and in the future. AgBioForum 12: 346-357.
18. Ehleringer J (1983) Ecophysiology of Amaranthus palmeri, a sonoran desert summer annual. Oecologia 57: 107-112.
19. Franssen AS, Skinner DZ, Al-Khatib K, Horak MJ, Kulakow PA (2001) Interspecific hybridization and gene flow of ALS resistance in Amaranthus species. Weed Sci 49: 598-606.
20. Gaines TA (2009) Molecular genetics of glyphosate resistance in Palmer amaranth (Amaranthus palmeri L.). Ph. D. Dissertation, Colorado State University, Fort Collins.
21. Gaines TA, Zhang W, Wang D, Bukun B, Chisholm ST, Shaner DL, Nissen SJ, Patzoldt WL, Tranel PJ, Culpepper AS, Grey TL, Webster TM, Vencill WK, Sammons RD, Jiang J, Preston C, Leach JE, Westra P (2010) Gene amplification confers glyphosate resistance in Amaranthus palmeri. Proc Natl Acad Sci USA 107: 1029-1034.
22. Gaines TA, Shaner DL, Ward SM, Leach JE, Preston C, Westra P (2011) Mechanism of resistance of evolved glyphosate-resistant Palmer amaranth (Amaranthus palmeri). J Agric Food Chem 59: 5886-5889.
23. Gaines TA, Ward SM, Bukun B, Preston C, Leach JE, Westra P (2012) Interspecific hybridization transfers a previously unknown glyphosate resistance mechanism in Amaranthus species. Evol Appl 5: 29-38.
24. Gaines TA, Wright AA, Molin WT, Lorentz L, Riggins CW, Tranel PJ, Beffa R, Westra P, Powles SB (2013) Identification of genetic elements associated with EPSPS gene amplification. PLoS One 8: e65819.
25. Gardner JG, Nelson GC (2008) Herbicides, glyphosate-resistance and acute mammalian toxicity: simulating an environmental effect of glyphosate-resistant weeds in the USA. Pest Manag Sci 64: 470-478.
26. Ge X, d'Avignon DA, Ackerman JJH, Sammons RD (2010) Rapid vacuolar sequestration: the horseweed glyphosate resistance mechanism. Pest Manag Sci 66: 345-348.
27. 31P NMR. Pest Manag Sci 67: 1215-1221.
28. 31P NMR investigation. J Agric Food Chem 60: 1243-1250.
29. Grant WF (1959a) Cytogenetic studies in Amaranthus. III. Chromosome numbers and phylogenetic aspects. Can J Genet Cytol 1: 313-328.
30. Grant WF (1959b) Cytogenetic studies in Amaranthus. I. Cytological aspects of sex determination in dioecious species. Can J Bot 37: 413-417.
31. Green JM (2009) Evolution of glyphosate-resistant crop technology. Weed Sci 57: 108-117.
32. Gustafsson A (1947) Apomixis in higher plants. III. Biotype and species formation. Lunds Univ Arsskr 43: 71-178.
33. Heap I (2013) International Survey of Herbicide Resistant Weeds. Online. Internet. www. weedscience. org. Accessed 7 August 2013.
34. Jacobsen P (1957) The sex chromosoes in Humulus L. Hereditas 43: 357-370.
35. Jalaludin A, Han H, Powles S (2013) Evolution in action: a double amino acid substitution in the EPSPS gene endows high-level glyphosate resistance. In: Proceedings of the global herbicide resistance challenge conference, Perth, p 35.
36. James C (2012) 2012 ISAAA report on global status of Biotech/GM Crops. International Service for the Acquisition of Agri-Biotech Applications Brief 44-2012, Ithaca.
37. Jha P, Norsworthy JK, Riley MB, Bridges W (2010) Shade and plant location effects on germination and hormone content of Palmer amaranth (Amaranthus palmeri) seed. Weed Sci 58: 16-21.
38. Keeley PE, Carter CH, Thullen RM (1987) Influence of planting date on growth of Palmer amaranth (Amaranthus palmeri). Weed Sci 35: 199-204.
39. Kleter GA, Kuiper HA (2003) Environmental fate and impact considerations related to the use of transgenic crops. In: Voss G, Ramos G (eds) Chemistry of plant protection. Wiley-VCH, Weinheim, pp 304-321.
40. Lanoue KZ, Wolf PG, Browning S, Hood EE (1996) Phylogenetic analysis of restriction-site variation in wild and cultivated Amaranthus species (Amaranthaceae). Theor Appl Genet 93: 722-732.
41. Lata H, Chandra S, Techen N, Khan IA, ElSohly MA (2010) Assessment of the genetic stability of micropropagated plants of Cannabis sativa by ISSR markers. Planta Med 76: 97-100.
42. Lata H, Chandra S, Techen N, Khan IA, ElSohly MA (2011) Molecular analysis of genetic fidelity in Cannabis sativa L. plants grown from synthetic (encapsulated) seeds following in vitro storage. Biotech Lett 33: 2503-2508.
43. Lebrun M, Sailland A, Freyssinet G (1997) Mutated 5-enol pyruvylshikimate-3-phosphate synthase, gene coding for said protein and transformed plants containing said gene. World Patent Application No. WO9704103.
44. Lee TT (1984) Release of lateral buds from apical dominance by glyphosate in soybean and pea seedlings. J Plant Growth Regul 3: 227-235.
45. Lee RM, Thimmapuram J, Thinglum KA, George G, Hernandez AG, Wright CL, Klim RW, Mikel MA, Tranel PJ (2009) Sampling the waterhemp (Amaranthus tuberculatus) genome using pyrosequencing technology. Weed Sci 57: 463-469.
46. Ma GG, Park YJ, Lee GA, Lee JR, Lee SY, Kwak JG, Kim TS, Cho EG (2008) SSR primer sets for identification of Amaranth species. Rep Korean Kongkae Taeho Kongbo Patent Oct 18, 2008, KR 2008092187, A20081015.
47. Massinga RA, Currie RS, Horak MJ, Boyer J (2001) Interference of Palmer amaranth in corn. Weed Sci 49: 202-208.
48. Mayo CM, Horak MJ, Peterson DE, Boyer JE (1995) Differential control of four Amaranthus species by six postemergence herbicides in soybean (Glycine max). Weed Technol 9: 141-147.
49. Morgan GD, Baumann PA, Chandler JM (2001) Competitive impact of Palmer amaranth (Amaranthus palmeri) on cotton (Gossypium hirsutum) development and yield. Weed Technol 15: 408-412.
50. Nandula VK, Reddy KN, Koger CH, Poston DH, Rimando AM, Duke SO, Bond JA, Ribeiro DN (2012) Multiple resistance to glyphosate and pyrithiobac in Palmer amaranth (Amaranthus palmeri) from Mississippi and response to flumiclorac. Weed Sci 60: 179-188.
51. Ng CH, Wickneswary R, Salmijah S, Teng YT, Ismail BS (2003) Gene polymorphisms in glyphosate-resistant and -susceptible biotypes of Eleusine indica from Malaysia. Weed Res 43: 108-115.
52. Parker JS, Clark MS (1991) Dosage sex-chromosome systems in plants. Plant Sci 80: 79-92.
53. Perez-Jones A, Mallory-Smith C (2010) Biochemical mechanisms and molecular basis of evolved glyphosate resistance in weed species. In: Nandula VK (ed) Glyphosate resistance in crops and weeds. Wiley, Hoboken, pp 119-140.
54. Pline-Srnic W (2006) Physiological mechanisms of glyphosate resistance. Weed Technol 20: 290-300.
55. Popa G, Cornea CP, Ciuca M, Babeanu N, Popa O, Marin D (2010) Studies on genetic diversity in Amaranthus species using the RAPD markers. Analele Universitǎtii din Oradea-Fascicula Biologie 17: 280-285.
56. Powles SB, Lorraine-Colwill DF, Delow JJ, Preston C (1998) Evolved resistance to glyphosate in rigid ryegrass (Lolium rigidum) in Australia. Weed Sci 46: 604-607.
57. Pratley J, Urwin N, Stanton R, Baines P, Broster J, Cullis K, Schafer D, Bohn J, Krueger R (1999) Resistance to glyphosate in Lolium rigidum. I. Bioevaluation. Weed Sci 47: 405-411.
58. Salas RA, Dayan FE, Pan Z, Watson SB, Dickson JW, Scott RC, Burgos NR (2012) EPSPS gene amplification in glyphosate-resistant Italian ryegrass (Lolium perenne ssp. multiflorum) from Arkansas. Pest Manag Sci 68: 1223-1230.
59. Sammons RD, Meyer J, Hall E, Ostrander E, Schrader S (2007) A simple continuous assay for EPSP synthase from plant tissue. http://www. cottoninc. com/2007-Glyphosate-Resistant-Palmer-Amaranth/11a-Industry-Sammons-NCWSS07-poster. pdf. Accessed 20 January 2012.
60. Seefeldt SS, Jensen JE, Fuerst EP (1995) Log-logistic analysis of herbicide dose-response relationships. Weed Technol 9: 218-227.
61. Selmecki A, Gerami-Nejad M, Paulson C, Forche A, Berman J (2008) An isochromosome confers drug resistance in vivo by amplification of two genes, ERG11 and TAC1. Mol Microbiol 68: 624-641.
62. Shaner DL, Nadler-Hassar T, Henry WB, Koger CH (2005) A rapid in vivo shikimate accumulation assay with excised leaf discs. Weed Sci 53: 769-774.
63. Siehl DL, Subramaniam MV, Walters EW, Blanding JH, Niderman T, Weinmann C (1997) Evaluating anthranilate synthase as a herbicide target. Weed Sci 45: 628-633.
64. Sosnoskie LM, Webster MTM, Kichler JM, MacRae AW, Grey TL, Culpepper AS (2012) Pollen-mediated dispersal of glyphosate-resistance in Palmer amaranth under field conditions. Weed Sci 60: 366-373.
65. Steinau AN, Skinner DZ, Steinau M (2003) Mechanism of extreme genetic recombination in weedy Amaranthus hybrids. Weed Sci 51: 696-701.
66. Steinrücken H, Amrhein N (1980) The herbicide glyphosate is a potent inhibitor of 5-enolpyruvylshikimic acid-3-phosphate synthase. Biochem Biophys Res Com 94: 1207-1212.
67. Trucco F, Jeschke MR, Rayburn AL, Tranel PJ (2005) Promiscuity in weedy amaranths: high frequency of female tall waterhemp (Amaranthus tuberculatus) × smooth pigweed (A. hybridus) hybridization under field conditions. Weed Sci 53: 46-54.
68. Trucco F, Zheng D, Woodyard AJ, Walter JR, Tatum TC, Rayburn AL, Tranel PJ (2007) Nonhybrid progeny from crosses of dioecious Amaranths: implications for gene-flow research. Weed Sci 55: 119-122.
69. Wassom JJ, Tranel PJ (2005) Amplified fragment length polymorphism-based genetic relationships among weedy Amaranthus species. J Hered 96: 410-416.
70. Watson S (1877) Descriptions of new species of plants, with revisions of certain genera. Proc Am Acad Arts Sci 12: 246-278.
71. Webb MR (1992) A continuous spectrophotometric assay for inorganic phosphate and for measuring phosphate release kinetics in biological systems. Proc Natl Acad Sci USA 89: 4884-4887.
72. Westergaard M (1958) The mechanism of sex determination in dioecious plants. Adv Genet 9: 217-281.
73. Wetzel DK, Horak MJ, Skinner DZ (1999) Use of PCR-based molecular markers to identify weedy Amaranthus species. Weed Sci 47: 518-523.
74. Wiersma A (2012) Regional whole plant and molecular response of Kochia scoparia to glyphosate. M. S. thesis, Colorado State University, p 55.
75. Xu ZL, Ali Z, Yi JX, He XL, Zhang DY, Yu GJ, Khan AA, Khan IA, Ma HX (2011) Expressed sequence tag-simple sequence repeat-based molecular variance in two Salicornia (Amaranthaceae) populations. Genet Mol Res 10: 1262-1276.