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( 12 ) United States Patent US010392630B2 (12 ) United States Patent ( 10 ) Patent No. : US 10 , 392 ,630 B2 Aponte et al. (45 ) Date of Patent: Aug. 27 , 2019 ( 54 ) PLANTS HAVING INCREASED TOLERANCE (56 ) References Cited TO HERBICIDES U . S . PATENT DOCUMENTS ( 71 ) Applicant: BASF AGRO B . V ., EA Arnheim (NL ) 5 , 169 ,770 A 12 / 1992 Chee et al . 5 , 198 ,013 A 3 / 1993 Hirai et al. (72 ) Inventors : Raphael Aponte , Mannheim (DE ) ; 5 , 322 , 783 A 6 / 1994 Tomes et al. 5 , 366 , 892 A 11/ 1994 Foncerrada et al. Stefan Tresch , Kirchheim (DE ) ; 5 , 376 ,543 A 12 / 1994 Chee et al. Matthias Witschel , Bad Duerkheim 5 , 380 ,831 A 1 / 1995 Adang et al. (DE ); Jens Lerchl, Golm (DE ) ; Dario 5 ,436 , 391 A 7 / 1995 Fujimoto et al . Massa , Mannheim (DE ) ; Tobias Seiser , 5 , 485 , 192 A 1 / 1996 Nagahata et al . Mannheim (DE ) ; Thomas Mietzner , 5 , 593 , 881 A 1 / 1997 Thompson et al . 5 , 723 , 756 A 3 / 1998 Peferoen et al. Annweiler (DE ) ; Jill Marie Paulik , 5 , 737 ,514 A 4 / 1998 Stiffler Cary , NC (US ) ; Chad Brommer , 5 , 747 , 450 A 5 / 1998 Ohba et al . Raleigh , NC (US ) 5 , 767 , 373 A 6 / 1998 Ward et al. 5 , 773 ,702 A 6 / 1998 Penner et al. 5 , 859 , 348 A 1 / 1999 Penner et al. ( 73 ) Assignee : BASF AGRO B . V . , Arnhem (NL ) 5 , 939 , 360 A 8 / 1999 Adachi et al . 5 ,939 ,602 A 8 / 1999 Volrath et al . ( * ) Notice : Subject to any disclaimer, the term of this 5 , 948 , 917 A 9 / 1999 Adachi et al. patent is extended or adjusted under 35 5 , 990 , 387 A 11/ 1999 Tomes et al . 6 ,018 , 105 A 1 / 2000 Johnson et al. U . S . C . 154 (b ) by 0 days . 6 ,027 , 945 A 2 / 2000 Smith et al . 6 ,084 , 155 A 7 / 2000 Volrath et al . (21 ) Appl. No. : 14 /911 , 814 6 , 160 , 206 A 12 / 2000 Sato et al . 6 , 308 ,458 B1 10 / 2001 Volrath et al. Aug . 12 , 2014 6 , 368 , 800 B1 4 /2002 Smith et al. ( 22 ) PCT Filed : 6 ,653 , 529 B2 11 /2003 Peng et al . ( 86 ) PCT No. : PCT/ IB2014 / 063877 (Continued ) $ 371 (c ) ( 1 ) , FOREIGN PATENT DOCUMENTS ( 2 ) Date : Feb . 12 , 2016 CA 2382090 A1 2 / 2001 (87 ) PCT Pub. No. : W02015 /022640 CA 2807035 AL 2 / 2012 PCT Pub . Date : Feb . 19 , 2015 (Continued ) (65 ) Prior Publication Data OTHER PUBLICATIONS Maniatis et al. , 1982 , Molecular Cloning : A Laboratory Manual , US 2016 /0201078 A1 Jul. 14 , 2016 Cold Spring Harbor Laboratory , pp . 324 - 343 and 387 -389 . * Keskin et al . , 2004 , Protein Science 13 : 1043 - 1055 . * Guo et al. , 2004 , Proceedings of the National Academy of Sciences Related U . S . Application Data USA 101 : 9205 - 9210 . * Thornton et al. , 2000 , Nature Structural Biology , structural genomic ( 60 ) Provisional application No . 61/ 866 , 067, filed on Aug . supplement , Nov. 2000 : 991 - 994 . * 15 , 2013 , provisional application No . 61/ 864, 671 , Brachypodium distachyon protoporphyrinogen oxidase with UniProt filed on Aug. 12 , 2013 , provisional application No . accession No. I1IZ42 , published on Jun . 13 , 2012 . * 61/ 864, 672 , filed on Aug. 12 , 2013 . Koch et al. , 2004 , EMBO J . 23 : 1720 - 1728 . * (Continued ) (51 ) Int. Ci. C12N 15 / 82 ( 2006 . 01 ) Primary Examiner — Bratislav Stankovic AOIN 37 / 48 ( 2006 .01 ) (74 ) Attorney, Agent, or Firm — Marshall , Gerstein & AOIN 43 /54 ( 2006 .01 ) Borun LLP A01N 43 /653 ( 2006 .01 ) (57 ) ABSTRACT A01N 43 /84 ( 2006 . 01 ) The invention refers to plants comprising wild -type or AOIN 57/ 16 ( 2006 . 01 ) mutated Alopecurus PPO enzymes, and methods of obtain C12N 9 / 02 ( 2006 .01 ) ing such plants . The present invention further refers to a (52 ) U .S . CI. method for controlling weeds at a plant cultivation site , the CPC .. .. .. C12N 15 /8274 ( 2013 .01 ) ; A01N 37 / 48 method comprising the steps of providing , at said site , a ( 2013 .01 ) ; AOIN 43 / 54 (2013 .01 ) ; AOIN plant that comprises at least one nucleic acid comprising a 43 /653 (2013 .01 ) ; AOIN 43 /84 ( 2013 .01 ) ; nucleotide sequence encoding a wild - type or a mutated AOIN 57/ 16 ( 2013 .01 ) ; C12N 9 /001 Alopecurus PPO enzyme which is resistant or tolerant to a ( 2013 .01 ) ; C12N 9 /0071 ( 2013 .01 ) ; C12Y PPO - inhibiting herbicide by applying to said site an effec 103 /03004 ( 2013 .01 ) tive amount of said herbicide . (58 ) Field of Classification Search None 7 Claims, 6 Drawing Sheets See application file for complete search history . Specification includes a Sequence Listing . US 10 ,392 ,630 B2 Page 2 (56 ) References Cited WO WO - 2015 /022636 A2 2 / 2015 WO W O - 2015 /022639 A2 2 / 2015 U . S . PATENT DOCUMENTS WO WO - 2015 /092706 A1 6 / 2015 6 ,905 , 852 B1 6 / 2005 Horikoshi et al . 7 ,671 , 254 B23 / 2010 Tranel et al . OTHER PUBLICATIONS 7 ,705 ,200 B2 4 / 2010 Dam et al . Arnould et al. , The domain structure ofprotoporphyrinogen oxidase , 7 ,745 ,699 B2 6 / 2010 Nakajima et al . the molecular target of diphenyl ether -type herbicides . Proc. Natl . 7 , 842 , 856 B2 11/ 2010 Tranel et al . 8 ,097 ,774 B2 1 / 2012 Hawkes et al. Acad . Sci. USA , 95 : 10553 - 8 (1998 ). 8 , 129 ,589 B2 3 / 2012 Tanaka et al. Che et al. , Molecular characterization and subcellular localization of 8 ,338 ,337 B2 12 / 2012 Song et al . protoporphyrinogen oxidase in spinach chloroplasts . Plant Physiol. 2003 /0236208 Al 12/ 2003 Kmiec et al. 124 : 59 - 70 ( 2000 ) . 2004 / 0082770 A1 4 /2004 Castle et al . Choi et al. , Generation of resistance to the diphenyl ether herbicide , 2005 /0084859 AL 4 / 2005 Nakajima et al . oxyfluorfen , via expression of the Bacillus subtilis protoporphyrinogen 2007 /0039067 A1 * 2 / 2007 Feldmann .. .. .. .. .. CO7K 14 /415 oxidase gene in transgenic tobacco plants . Biosci. Biotechnol. 800 / 278 Biochem . 62 ( 3 ) : 558 -60 ( 1998 ) . 2007 / 0050863 A1 3 / 2007 Tranel et al . Corradi et al. , Crystal structure of protoporphyrinogen oxidase from 2007 /0214515 Al 9 / 2007 Dam et al. Myxococcus xanthus and it complex with the inhibitor acifluorfen . 2009 / 0049567 A1 2 /2009 Olhoft et al . J Biol Chem . 281( 50 ) : 38625 - 33 ( 2006 ) . 2010 /0100988 Al Dayan et al ., Phytotoxicity of Protoporphyrinogen Oxidase Inhibi 4 / 2010 Tranel et al. tors : Phenomenology , Mode of Action and Mechanisms of Resis 2011 /0201501 A1 8 / 2011 Song et al . tance , Herbicide Activity : Toxicology , Biochemistry and Molecular 2012 /0122223 AL 5 / 2012 Gocal et al. Biology , eds. Roe et al. , pp . 11 - 35 ( 1997 ) . 2013 /0184155 Al 7 / 2013 Newton et al. Extended European Search Report , issued in co -assigned applica 2014 / 0123340 A1 5 / 2014 Aponte et al . tion No . 11848519 . 2 , dated Apr. 23 , 2014 . 2014 / 0189906 A1 7 / 2014 Gocal et al . GenBank Accession No. AX084732 , submitted on Mar. 9 , 2001 . 2015 / 0299725 Al 10 / 2015 Lerchl et al . Ha et al . , The plastidic Arabidopsis protoporphyrinogen IX oxidase 2016 /0194654 AL 7 / 2016 Aponte et al. gene, with or without the transit sequence , confers resistance to the 2016 / 0201078 AL 7 / 2016 Aponte et al . diphenyl ether herbicide in rice . Plant Cell Environ . 27 : 79 - 88 ( 2003 ) . FOREIGN PATENT DOCUMENTS Hanin et al ., Gene targeting in Arabidopsis . Plant J . 28 : 671 - 7 ( 2001 ) . CN 1150820 A 5 /1997 CN 1036571 C 12 / 1997 Hao et al. , Protoporphyrinogen oxidase inhibitor : An ideal target for CN 1212724 A 3 / 1999 herbicide discovery . Chimia , 65 ( 12 ) : 961 - 9 (2011 ) . CN 1175107 C 11/ 2004 Heinemann et al. , Functional definition of the tobacco CN 1894408 A 1 / 2007 protoporphyrinogen IX oxidase substrate -binding site . Biochem . J . CN 101215289 A 7 / 2008 402 : 575 - 80 ( 2007 ) . CN 101437844 A 5 /2009 Holmberg, A fine line : New herbicide - tolerant crops blur the fine CN 101998988 A 3 / 2011 line between weed control and crop injury . Successful Farm . 98 ( 5 ) : DE 19505995 A1 8 / 1996 25 - 7 (2000 ) . EP 0397687 Al 11 / 1990 Huang et al . , Synthesis and herbicidal activity of isoindoline - 1 , 3 EP 0424047 A1 4 / 1991 dione substituted benzoxazinone derivatives containing a carbox EP 0900795 A1 3 / 1999 WO WO - 93 /07256 Al 4 / 1993 ylic ester group . J . Agric . Food Chem . 57 : 9585 - 92 ( 2009 ) . WO WO - 95 / 34659 Al 12 / 1995 International Preliminary Report on Patentability , issued in PCT/ WO WO - 96 / 26202 A1 8 / 1996 IB2011 /055701 , dated Jun . 27 , 2013 . WO WO - 1997 / 004088 A1 2 / 1997 International Search Report , corresponding International Applica WO WO - 1997 /032011 A1 9 / 1997 tion No . PCT/ EP2013 / 062744 , dated Dec. 10 , 2014 . WO WO - 97 /41116 A1 11 / 1997 International Search Report, issued in PCT/ IB2011/ 055701 , dated WO WO - 97 /41117 A1 11 / 1997 May 3 , 2012 . WO WO - 97 /41118 Al 11 / 1997 Jung et al . , Dual targeting ofMyxococcus xanthus protoporphyrinogen WO WO - 1998 /029554 A1 7 / 1998 oxidase into chloroplasts and mitochondria and high level oxyfluorfen wo WO - 1998 /033927 A1 8 / 1998 resistance . Plant Cell Environ . 27 : 1436 - 46 ( 2004 ) . WO WO - 2001/ 012815 A1 2 / 2001 Jung et al. , Resistance mechanisms in protoporphyrinogen oxidase WO WO - 2001 /068826 A2 9 / 2001 WO WO -01 / 83459 A2 11 /2001 (PROTOX ) inhibitor- resistant transgenic rice . J . Plant Biol. 50 ( 3 ) : WO WO - 02 / 068607 A2 9 / 2002 586 - 94 ( 2007) . WO WO - 2005 / 107437 A2 11/ 2005 Koch et al. , Crystal structure of protoporphyrinogen IX oxidase : A WO WO - 2006 /024820 A1 3 / 2006 key enzyme in Haem and chlorophyll biosynthesis . EMBO J . 23 : WO WO - 2006 /037945 A1 4 / 2006 1720 - 8 ( 2004 ) . WO WO - 2007 /024739 A2 3 / 2007 Layer et al ., Structure and function of enzymes in Heme biosyn WO WO - 2007 /071900 Al 6 / 2007 thesis .
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