Fate of Herbicide Resistance Genes in Weeds - ACS Symposium

Chapter 24

Fate of Herbicide Resistance Genes in Weeds

H. Darmency and J. Gasquez

Downloaded by AUBURN UNIV on December 26, 2017 | http://pubs.acs.org Publication Date: February 23, 1990 | doi: 10.1021/bk-1990-0421.ch024

Laboratoire de Malherbologie, Institut National de la Recherche Agronomique, BV 1540, 21034 Dijon, Cedex, France

The appearance of herbicide resistance genes in weed populations may originate from mutations or genetic exchanges with other organisms. Using triazine resistance as an example, we attempted to answer several questions about the origin and the spread of genes for resistances in weed populations. We found that triazine resistant mutants do not appear at random, but are the result of particular genomes capable of producing a high number of mutants, which we refer to as a founder effect in each resistant population. However, the presence of the mutated chloroplast gene is not believed responsible for high levels of resistance in these weeds. We also believe that because of the high selection pressure conferred upon the resistant genes in herbicide treated areas, mutation events even at very low frequencies have high probabilities of evolving resistant plants, and that spread of resistance from engineered crop plants will likely occur in spite of cytoplasmic inheritance. During the last two decades, weed control techniques in Europe have been marked by four major features: the release of antigramineae herbicides in cereals; an increased selective control of perennials; a trend to use lower quantities of active ingredients; and the appearance of herbicide resistant weeds which is becoming increasingly important in crop production (1). The appearance of herbicide resistant weeds indicates a clearly adapted response of weeds to agricultural practices and has aided research in the development of herbicide resistant crops. This paper discusses the origins of herbicide resistance genes. HERBICIDE RESISTANCES Occurrence: The appearance of herbicide resistant weeds was predicted as early as 1950. Blackman (2) then pointed out the likenesses between mass selection for a given character in crops and selection of weeds after continuous herbicide treatments in fields. Herbicide resistance has been reported worldwide in a wide variety of crops that involve herbicide families with different modes of action and several weeds species (1). 0097-6156/90/0421-0353$06.00/0 © 1990 American Chemical Society

Green et al.; Managing Resistance to Agrochemicals ACS Symposium Series; American Chemical Society: Washington, DC, 1990.

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MANAGING RESISTANCE TO AGROCHEMICALS


However, c o n t r a r y t o t h e p r e d i c t i o n t h a t assumes the i n v o l v e m e n t o f many genes, t h e g e n e t i c c o n t r o l o f the f o l l o w i n g r e s i s t a n c e s i s d e t e r m i n e d by o n l y one o r a few genes: t r i a z i n e s ( l o s s of h e r b i c i d e b i n d i n g due t o a c h l o r o p l a s t m u t a t i o n ( 3 ) ) , b i p y r i d i l i u m ( s i n g l e gene c o n t r o l o f the amount o f t h r e e d e t o x i c a t i o n enzymes ( 4 ) ) , and d i n i t r o a n i l i n e r e s i s t a n c e s ( u n a f f e c t e d m i c r o t u b u l e f o r m a t i o n due t o t u b u l i n m u t a t i o n ( 5 ) ) . The g e n e t i c s f o r d i c l o f o p methyl ( 6 ) , c h l o r o t o l u r o n ( 7 ) , mecoprop ( 8 ) , and t r i a l l a t e r e s i s t a n c e s (9) a r e s t i l l not c l e a r . Other c a s e s o f d i f f e r e n t i a l t o l e r ance i n r e s p o n s e t o h e r b i c i d e s a r e known among d i f f e r e n t b i o t y p e s i n s e v e r a l s p e c i e s (10) but a r e not c l e a r l y r e l a t e d t o t h e s e l e c t i o n of r e s i s t a n t p l a n t s i n the f i e l d . Problems and Model: I f t h e development o f h e r b i c i d e r e s i s t a n c e c o n t i n u e s , the l i f e s p a n o f s e v e r a l h e r b i c i d e s w i l l p r o b a b l y be s h o r t e n e d , l e a v i n g f a r m e r s t o f a c e s e v e r a l i m p o s s i b l e weed c o n t r o l problems. Moreover, weeds r e s i s t a n t t o h e r b i c i d e s a r e c o s t l y because a l t e r n a t i v e h e r b i c i d e s a r e not always a v a i l a b l e . In some c a s e s , s u p p l e m e n t a r y t r e a t m e n t s must be a p p l i e d i n a d d i t i o n t o t h e s t a n d a r d t r e a t m e n t t h a t remains e f f i c i e n t f o r c o n t r o l l i n g numerous " o r d i n a r y " weeds. Of the 3 m i l l i o n h e c t a r e s o f c o r n grown i n F r a n c e , 1.2 m i l l i o n h e c t a r e s a r e now s u b j e c t e d t o a postemergence treatment (e.g., p y r i d a t e ) s p e c i f i c a l l y d i r e c t e d against t r i a z i n e r e s i s t a n t weeds. Thus, t h i s s o - c a l l e d " r e m e d i a l t r e a t m e n t " i s becoming a s t a n d a r d t r e a t m e n t t h a t i s c a r r i e d out a f t e r t h e p r e emergence a t r a z i n e t r e a t m e n t . This creates a f o u r - f o l d increase i n the c o s t o f weed c o n t r o l i n t h e s e c o r n f i e l d s . The r e d u c e d e f f i c a c y o f c e r t a i n h e r b i c i d e s and t h e i n c r e a s e d c o s t o f weed management a r e two r e a s o n s t o s t u d y t h e appearance o f h e r bicide resistant plants. In a d d i t i o n , fundamental knowledge o f p l a n t . p o p u l a t i o n b i o l o g y i s a l s o a concern. In c o n t r a s t w i t h most e c o l o g i c a l f a c t o r s , h e r b i c i d e t r e a t m e n t i s one o f the r a r e s e l e c t i o n pressures t h a t i s easy t o study w i t h i n a genuine e n v i ronment. B i o l o g i s t s can u n d e r s t a n d and t e s t by e x p e r i m e n t a l methods t h e l o n g - t e r m e f f e c t s o f f i e l d a p p l i e d h e r b i c i d e s on weed populations. Hence, t h e weed p o p u l a t i o n / h e r b i c i d e model i s an e x c e l l e n t example f o r s t u d y i n g a d a p t a t i o n and e v o l u t i o n . T h e r e f o r e , a l l o f t h e o p e r a t i v e f a c t o r s c o n t r i b u t i n g t o t h e appearance o f r e s i s t a n t p l a n t s i n a p o p u l a t i o n o r a s p e c i e s s h o u l d be precisely defined. The g e n e t i c s o f weed s p e c i e s a r e c e r t a i n l y t h e f i r s t a r e a s t h a t must be i n v e s t i g a t e d . Q u e s t i o n s t o be r a i s e d t o s t u d y weed g e n e t i c s i n c l u d e : 1. 2. 3. 4.

Does m u t a t i o n o c c u r a t random? Does a s p e c i a l g e n e t i c s t r u c t u r e o f weed p o p u l a t i o n s e x i s t i n t h o s e p o p u l a t i o n s e v o l v i n g toward r e s i s t a n c e ? How does t h e r e g u l a t i o n o f r e s i s t a n c e genes work? What a r e t h e r i s k s o f gene t r a n s f e r a s s o c i a t e d w i t h the r e l e a s e o f g e n e t i c a l l y improved r e s i s t a n t c r o p s ?

T r i a z i n e Resistance: We a t t e m p t e d t o answer t h e p r e v i o u s f o u r q u e s t i o n s u s i n g d a t a and examples d e r i v e d from the s t u d y o f t h e b e s t documented c a s e o f h e r b i c i d e r e s i s t a n c e , t r i a z i n e r e s i s t a n c e . Two k i n d s o f mechanisms may be r e s p o n s i b l e f o r t h i s t r i a z i n e r e s i s t a n c e ; f i r s t i s t h e p r e s e n c e o f d e t o x i f i c a t i o n m e t a b o l i c pathways, as s e e n i n c o r n ( 1 1 ) . T h i s a l s o may o c c u r i n weed p o p u l a t i o n s , e s p e c i a l l y P a n i c o i d e a e , but a low h e r i t a b i l i t y makes i t s s t u d y complex. The s e c o n d mechanism o f t r i a z i n e r e s i s t a n c e i s the l o s s o f h e r b i c i d e b i n d i n g a t the l e v e l o f the c h l o r o p l a s t .


24.

DARMENCY AND GASQUEZ

Fate of Herbicide Resistance Genes in Weeds 355

T h i s s e c o n d mechanism i s due t o a p o i n t m u t a t i o n a t t h e c h l o r o p l a s t gene e n c o d i n g f o r a Photosystem I I 32 KD membrane p r o t e i n ( 3 ) . T h i s p o i n t m u t a t i o n i s the r e s u l t o f a change o f one a m i n o - a c i d r e s i d u e and the subsequent l o s s o f t h e p r o t e i n - h e r b i c i d e a f f i n i t y . R e s i s t a n t c h l o r o p l a s t s a r e 1 , 0 0 0 - f o l d more r e s i s t a n t t h a n s u s c e p t i b l e c h l o r o p l a s t s , when a s s a y e d i n v i t r o . Whole p l a n t s a l s o show a t l e a s t a 2 0 0 - f o l d i n c r e a s e d r e s i s t a n c e , which c o n f e r s a c l e a r , s e l e c t i v e advantage i n t r i a z i n e t r e a t e d f i e l d s , o r c h a r d s and v i n e yards (13). E v i d e n c e t h a t a s p e c i f i c gene i s r e s p o n s i b l e f o r r e s i s t a n c e was p r o v e n by t h e p r o d u c t i o n o f t o l e r a n t t r a n s g e n i c tobacco (12). Now, n e a r l y 50 s p e c i e s a r e known t o have a t l e a s t one t r i a z i n e r e s i s t a n t p o p u l a t i o n and s e v e r a l m i l l i o n h e c t a r e s i n more t h a n 15 c o u n t r i e s a r e i n f e c t e d w i t h t r i a z i n e r e s i s t a n t weed populations (1).


SPONTANEOUS MUTANTS I t i s i n t r i g u i n g t h a t a l l t r i a z i n e r e s i s t a n t b i o t y p e s i n which c h l o r o p l a s t DNA has been a n a l y z e d a r e mutated a t t h e same p o s i t i o n on t h e psbA gene on the c h l o r o p l a s t DNA ( T a b l e I ) . T h i s m u t a t i o n c o r r e s p o n d s t o t h e change o f one a m i n o - a c i d a t P o s i t i o n 264 o f t h e psbA gene p r o d u c t , the 32 KD p r o t e i n . The f a c t t h a t t h e m u t a t i o n o c c u r s on t h e psbA gene i s n o t s u r p r i s i n g because a t r a z i n e i s a c o m p e t i t o r o f q u i n o n e s b i n d i n g t o t h e 32 KD p r o t e i n . However, t h e r e a s o n f o r the e x c l u s i v e i n v o l v e m e n t o f P o s i t i o n 264 i n t h i s r e s i s t a n c e i n h i g h e r p l a n t s i s not known. Other m u t a t i o n s a t t h e psbA gene a r e known t o c o n f e r a t r a z i n e r e s i s t a n c e i n some organisms e.g., i n t h e a l g a e Chiamydomonas (14, 15). T h i s i n d i c a t e s t h a t a d i v e r s i t y o f mutants c o u l d have been expected. From t h e d a t a now a v a i l a b l e , i t appears t h a t 14 mutants a r e a l t e r e d a t P o s i t i o n 264 out o f 21 DNA a n a l y s e s o f t r i a z i n e r e s i s t a n t organisms ( T a b l e I ) . T h e r e f o r e , mutants a t o t h e r p o s i t i o n s may have t h e o r e t i c a l f r e q u e n c i e s between 15% and 59% (proba b i l i t y of 95%). To e x p l a i n t h e h i g h e r f r e q u e n c y o f mutants a t P o s i t i o n 264, i n s p i t e o f t h e lower f i t n e s s a s s o c i a t e d w i t h i t ( 1 6 ) , we i n v e s t i g a t e d whether some g e n e t i c mechanism i n c r e a s e d t h e chance o f t h i s m u t a t i o n . Such a mechanism, was i l l u s t r a t e d i n Chenopodium album and may p r o v i d e some l i g h t on t h e appearance o f c h l o r o p l a s t mutants. Precursor Plants: Rare e v e n t s i n p o p u l a t i o n s g e n e r a l l y cannot be d e t e c t e d u n l e s s 1,000 o r more i n d i v i d u a l s a r e a n a l y z e d from e a c h location. However, we p r o c e e d e d i n a s l i g h t l y d i f f e r e n t manner. S e e d l i n g s o f C. album were c o l l e c t e d i n a r e a s t h a t have n e v e r been treated with chemicals. When t r a n s p l a n t e d i n a greenhouse, one l e a f p e r p l a n t was c u t o f f and l e f t t o a b s o r b a t r a z i n e i n t h e d a r k and t h e n t h e amounts o f c h l o r o p h y l l f l u o r e s c e n c e were r e c o r d e d . The r e s u l t s o f t h i s t e s t i n d i c a t e d t h a t a l l p l a n t s were s u s c e p t i b l e to a t r a z i n e (Figure 1). The p l a n t s s e t seeds and t h e seeds from one p l a n t formed a f a m i l y . Then a t l e a s t 100 seeds o f e a c h f a m i l y were sown and a n a l y z e d f o r f l u o r e s c e n c e . Of t h e 869 f a m i l i e s d e r i v e d from p l a n t s c o l l e c t e d i n f i v e p o p u l a t i o n s ( T a b l e I I ) , 33 showed a t l e a s t one s e e d l i n g w i t h an i n t e r mediary f l u o r e s c e n c e curve ( F i g u r e 1 ( 2 1 ) ) . These s e e d l i n g s p r o v e d l a t e r t o have t h e mutated psbA gene a t P o s i t i o n 264 (19) and were moderately r e s i s t a n t to a t r a z i n e . They were c a l l e d Type I ( f o r i n t e r m e d i a t e l e v e l o f r e s i s t a n c e ) . The 33 mother p l a n t s and t h e i r c o r r e s p o n d i n g s e e d f a m i l i e s were c a l l e d Sp. because t h e y were s p e c i a l s u s c e p t i b l e p l a n t s t h a t p r o d u c e d mutant p l a n t s .


356


TABLE I :

MUTATION FOR ATRAZINE RESISTANCE

Resistance Level

Species


Higher

Plants Amaranthus b o u c h o n i i A. c r u e n t u s A. h y b r i d u s A. r e t r o f l e x u s B r a s s i c a napus Bromus t e c t o r u m Chenopodium album P h a l a r i s paradoxa Poa annua Senecio v u l g a r i s Solanum nigrum

Mutation

Reference

>500 >500 >500 >500 >500 >500 >500 >500 >500 >500 >500

psbA psbA psbA psbA psbA psbA psbA psbA psbA psbA psbA

264 264 264 264 264 264 264 264 264 264 264

17 17 17 3 18 17 19 20 21 17 22,

84 15 15 25 2 10 2 7 70 100

psbA psbA psbA psbA psbA psbA psbA psbA psbA psbA

264 256 255 251 219 264 219 211 264 211-251

24 25 25 15 25 26 27 27

Others Chlamydomonas r e i n h a r d t i i C. r e i n h a r d t i i C. r e i n h a r d t i i C. r e i n h a r d t i i C. r e i n h a r d t i i Synechococcus s p . S. s p . S. s p . Synechocystis Synechocystis *G. A j l a n i ; C. A s t i e r ,

TABLE I I :

* *

p e r s o n a l communication.

OCCURRENCE OF MUTANT PRECURSOR PLANTS IN POPULATIONS

Population

Origin

No. o f Families

No. o f Sp. Families

Burgundy B Burgundy C Burgundy D Alpes A l A l p e s A2

Garden Garden Garden Garden Garden

180 191 166 187 145

8 17 1 5 2

Mean % o f 1 Mutants w i t h i n Sp. F a m i l i e s 5.3 3.2 1.1 1.6 1.7



24.



F i g u r e 1 . F l u o r e s c e n c e c u r v e o f whole l e a v e s o f t h e t h r e e p h e n o t y pes o f Chenopodium album a f t e r a one n i g h t i n c u b a t i o n w i t h 30 ppm atrazine


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A M u t a t o r System: The Sp. f a m i l i e s p r o b a b l y d i s p l a y a p e c u l i a r genome because t h e y show an a v e r a g e Type I m u t a t i o n f r e q u e n c y as h i g h as 3.3%. T h i s i s much g r e a t e r t h a n t h e m u t a t i o n r a t e e x p e c t e d due t o chance a l o n e . A r n t z e n and D u e s i n g (29) p r e v i o u s l y s u g g e s t e d t h a t a m u t a t i o n f o r a t r a z i n e r e s i s t a n c e c o u l d have r e s u l t e d from a s p e c i f i c mutator system. I n t h e i r system, a h i g h f r e q u e n c y o f v a r i e g a t e d p l a n t s were o b t a i n e d . The s u g g e s t e d mutator system c o u l d p r o b a b l y be r e s p o n s i b l e f o r o t h e r t y p e s o f m u t a t i o n s a t t h e c h l o r o p l a s t l e v e l , but a p p r o p r i a t e s c r e e n i n g s ( e . g . , t h e wide use o f a t r a z i n e i n f i e l d s ) have n o t been u s e d . I f t r u e , t h i s mutator system c o u l d be t h e s t a r t i n g p o i n t f o r numerous r e s i s t a n c e s t o d i f f e r e n t h e r b i c i d e s . The e v o l u t i o n o f c r o s s - r e s i s t a n c e s c o u l d t h e r e f o r e be e x p e c t e d t o o c c u r w i t h i n a s h o r t t i m e . I n a d d i t i o n , we o b s e r v e d t h a t Type I mutants have a l l o f t h e i r psbA gene c o p i e s mutated (99.9% p r o b a b i l i t y ) w h i l e no h e t e r o p l a s m i c i t y was f o u n d i n Sp. p l a n t s ( 1 9 ) . T h i s i n d i c a t e s t h a t a mechanism o t h e r t h a n a h i g h m u t a t i o n r a t e must work t o a l l o w t h e r e l e a s e o f i n d i v i d u a l p l a n t s t h a t have t h e i r e n t i r e c h l o r o p l a s t p o p u l a t i o n mutated. T h i s c o u l d be due t o t h e c o n t r o l o f c h l o r o p l a s t DNA r e p l i c a t i o n d i r e c t e d by m i t o c h o n d r i a l o r n u c l e a r genomes. Indeed, a sequence homology has been f o u n d between m i t o c h o n d r i a l DNA and p a r t o f t h e c h l o r o p l a s t psbA gene. Moreover, t h i s homologous sequence i s e x p r e s s e d as an RNA t r a n s c r i p t i n a t r a z i n e r e s i s t a n t C. album o n l y and not i n t h e s u s c e p t i b l e p l a n t s ( 3 0 ) . Randomness: P r e d i c t i v e models f o c u s i n g on t h e appearance and s p r e a d o f r e s i s t a n t weeds g e n e r a l l y assume t h a t m u t a t i o n e v e n t s f i t a u n i f o r m s t a t i s t i c a l law, i . e . , t h a t i s t h e y o c c u r i n low f r e quencies at every l o c a t i o n . At b e s t , a normal d i s t r i b u t i o n o r normal laws a r e u s e d . In c o n t r a s t , weed r e s e a r c h on p o p u l a t i o n s t e a c h e s t h a t weed d i s t r i b u t i o n s i n s t e a d f i t c o n t a g i o u s (aggregat i v e ) laws ( 3 1 ) . In a d d i t i o n , the presence of s p e c i a l p r e c u r s o r p l a n t s t h a t p r o d u c e a h i g h f r e q u e n c y o f r e s i s t a n t mutants l e a d s us t o imagine a p a t c h y d i s t r i b u t i o n o f r e s i s t a n c e genes i n s p i t e o f a random r e p a r t i t i o n . T h i s i s important i n the case of p o l y g e n i c r e s i s t a n c e s because t h e p r o b a b i l i t y o f c o m b i n i n g two o r more genes i n one p l a n t by o u t c r o s s i n g may w i d e l y v a r y from l o c a t i o n t o l o c a t i o n because t h e f r e q u e n c y o f s i n g l e mutants may be v e r y d i f f e r ent . POPULATION STRUCTURE Monomorphism: An a d d i t i o n a l p i e c e o f e v i d e n c e i n f a v o r o f a p e c u l i a r genome f o r Sp. p l a n t s i s p r o v i d e d by isozyme a n a l y s e s o f two p o p u l a t i o n s from t h e Burgundy r e g i o n o f F r a n c e . The Sp. p l a n t s showed t h e same e l e c t r o p h o r e t i c p a t t e r n w h i l e 36 o t h e r p a t t e r n s were d e t e c t e d i n t h e p l a n t s t h a t do n o t c o n t a i n t h e Sp. genome i n t h e s e two p o p u l a t i o n s ( 3 2 ) . T h e r e f o r e , the p o t e n t i a l t o p r o d u c e mutants seems t o be r e s t r i c t e d t o o n l y one type o f p l a n t w i t h i n a given population. Of c o u r s e , t h i s c o u l d be s i m p l y c o i n c i d e n t a l and due t o a f o u n d e r e f f e c t . I n t h e p o p u l a t i o n s from t h e o t h e r r e g i o n s , t h e Sp. p l a n t s showed o t h e r e l e c t r o p h o r e t i c p a t t e r n s , i n d i c a t i n g t h a t t h e r e i s no r e l a t i o n s h i p between m u t a t i o n f r e q u e n c y and isozymes p r o d u c t i o n . The f a c t t h a t Type I mutants o r i g i n a t e from o n l y one t y p e o f p l a n t w i t h i n a p o p u l a t i o n i s c o r r o b o r a t e d by t h e monomorphic s t r u c t u r e o f a l l r e s i s t a n t p o p u l a t i o n s o f C^ album s t u d i e d i n F r a n c e and Canada (33, 3 4 ) . T h i s i s c e r t a i n l y the r e s u l t of a founder e f f e c t by one p l a n t o n l y . T h e r e a f t e r , a quick buildup of a population o c c u r r e d due t o t h e h i g h f i t n e s s v a l u e o f t h e r e s i s t a n t p l a n t i n a


24.




h e r b i c i d e t r e a t e d area. Monomorphism has been m a i n t a i n e d thanks t o low a l l o g a m y ( 5 % i n c o r n f i e l d s (35) and the i s o l a t i o n o f p o l l e n o u t s i d e the f i e l d . In c o n t r a s t , i f t h e l o c a t i o n i s s u i t a b l e f o r a h i g h s e e d m i g r a t i o n r a t e and a h i g h a l l o g a m y , a h i g h polymorphism l e v e l can be e x p e c t e d , as f o u n d i n a r e s i s t a n t p o p u l a t i o n o f A l o p e c u r u s myosuroides n e a r a r o a d s i d e i n I s r a e l ( C h a u v e l , INRA D i j o n , P e r s o n a l communication). Polymorphism: We p r e v i o u s l y s t u d i e d p o l y m o r p h i c r e s i s t a n t p o p u l a t i o n s o f Poa annua. In t h i s c a s e , a l l o g a m y was low (10% maximum i n the g r e e n h o u s e ) , but a p e c u l i a r f e a t u r e g r e a t l y enhanced t h e h y b r i d o u t p u t between t h e r e s i s t a n t p l a n t s and t h e a d j a c e n t s u s c e p t i b l e ones. The s e l e c t i o n p r e s s u r e due t o h a b i t a t e c o l o g y was h i d d e n f o r a t i m e due t o t h e d r a s t i c s e l e c t i o n p r e s s u r e due t o t h e h e r b i c i d e . The r e s i s t a n t p o p u l a t i o n d e v e l o p e d i n t h e c e n t r a l s t r i p o f a c i t y avenue, an a r e a open t o s e e d m i g r a t i o n and p r e v i o u s l y c o l o n i z e d by the annual e r e c t ecotype. By chance, t h e former r e s i s t a n t p l a n t i n t h i s a r e a was a p e r e n n i a l p r o s t r a t e e c o t y p e . Because l e a c h i n g o f a t r a z i n e t h r o u g h the s o i l was r a p i d , immigrant s u s c e p t i b l e p l a n t s ( m a i n l y a n n u a l e r e c t t y p e s ) grew and f l o w e r e d among r e s i s t a n t p l a n t s 5 o r 6 months a f t e r a h e r b i c i d e t r e a t m e n t . Isozyme a n a l y s i s i n d i c a t e d t h a t many h y b r i d s d e v e l o p e d ( 3 6 ) . The p o p u l a t i o n o f r e s i s t a n t Poa annua c o l o n i z i n g t h i s a r e a g r a d u a l l y e v o l v e d as an annual e r e c t . The d r a s t i c h e r b i c i d e s e l e c t i o n p r e s s u r e was h i d d e n f o r a time due t o the h a b i t a t e c o l o g y . T h i s d i s e q u i l i b r i u m was the s o u r c e o f t h e polymorphism. O r i g i n or Consequence: In l i g h t o f t h e s e s t u d i e s , i t appears t h a t t h e g e n e t i c s t r u c t u r e o f a r e s i s t a n t p o p u l a t i o n i s n o t t h e image o f t h e a n c e s t r a l s t r u c t u r e o f the p o p u l a t i o n from w h i c h r e s i s t a n t p l a n t s o r i g i n a t e d . T h e r e f o r e , i t i s d i f f i c u l t t o draw a c o n c l u s i o n about a p e c u l i a r g e n e t i c s t r u c t u r e p r o m o t i n g t h e appearance o f atrazine resistant plants. REGULATION OF

RESISTANCE

The f a c t t h a t p o p u l a t i o n s o r p l a n t s d i s p l a y r e s i s t a n c e genes i s n o t n e c e s s a r i l y synonymous w i t h t h e e x p r e s s i o n o f r e s i s t a n c e a t t h e whole p l a n t l e v e l . This i s c l e a r for polygenic resistances for w h i c h t h e a c c u m u l a t i o n o f two o r more genes i s n e c e s s a r y f o r a s u f f i c i e n t l e v e l of r e s i s t a n c e . This s i t u a t i o n a l s o occurs f o r atrazine resistance. The S e a r c h f o r R e s i s t a n t P l a n t s : The s e a r c h f o r Sp. and Type I mutant p l a n t s i n p o p u l a t i o n s from c u l t i v a t e d f i e l d s f a i l e d . These p l a n t s , as w e l l as many o t h e r t y p e s o f mutants may have been e l i m i n a t e d because c u l t i v a t i o n and o t h e r c u l t u r a l p r a c t i c e s have r e d u c e d t h e polymorphism o f f i e l d p o p u l a t i o n s ( 3 2 ) . Moreover, Type I mutants p r o b a b l y have a low f i t n e s s v a l u e i n the absence o f t r i a z i n e s (16). The f a c t t h a t mutants o r i g i n a t e from o n l y one o r v e r y few t y p e s o f i n d i v i d u a l s i n a p o p u l a t i o n r e p r e s e n t s a b o t t l e n e c k t o the spread of r e s i s t a n c e . Hence, r e s i s t a n c e c e r t a i n l y e v o l v e d i n fewer l o c a t i o n s t h a n c o u l d have been e x p e c t e d . F o r i n s t a n c e , no r e s i s t a n t C. album p l a n t s were found i n Burgundy w h i l e Sp. mother p l a n t s h a v i n g Type I d e s c e n d a n t s were f o u n d i n gardens i n Burgundy. A s e c o n d b o t t l e n e c k t o t h e s p r e a d o f t h e r e s i s t a n c e was f o u n d i n C. album p o p u l a t i o n s . The Type I mutants were r e s i s t a n t t o 0.5 kg a . i . / h a o n l y and 100% m o r t a l i t y was r e a c h e d w i t h 1 kg a . i . / h a ( 1 9 ) , w h i l e the a c t u a l dose u s e d i n c o r n f i e l d s was a t l e a s t 1.5 kg a . i . / h a ( t h e l e t h a l dose f o r s u s c e p t i b l e p l a n t s i s 0.1 kg a . i . / h a ) .


360



A p a r t from the chance o f h a v i n g a h e t e r o g e n e o u s h e r b i c i d e t r e a t m e n t l e a v i n g m i c r o - n i c h e s w i t h l e s s a t r a z i n e a p p l i e d i n some a r e a , and u n l e s s g e r m i n a t i o n o c c u r r e d l a t e i n the s e a s o n a f t e r p a r t i a l l e a c h i n g o r d e g r a d a t i o n o f t h e a t r a z i n e , Type I mutants a r e l i k e l y t o be k i l l e d . T h i s i n c o m p l e t e r e s i s t a n c e o f a psbA-mutated p l a n t b r i n g s up t h e q u e s t i o n o f how t h e t r u e r e s i s t a n t p l a n t s ( t h o s e t o l e r a t i n g more t h a n 40 kg a . i . / h a ) e v o l v e d . Lamarkism f o r R e s i s t a n c e : When g r o w i n g Type I mutants o f C. album f r e e o f any c h e m i c a l , t h e i r c h a r a c t e r i s t i c s ( l e t h a l dose an3 f l u o rescence curve) are m a t e r n a l l y i n h e r i t e d (28). However, when pest i c i d e s , i n c l u d i n g h e r b i c i d e s a t s u b l e t h a l d o s e s , a r e s p r a y e d on Type I s e e d l i n g s , t h e seeds o b t a i n e d from t h e s e p l a n t s g i v e i n d i v i d u a l s showing l e t h a l doses o f 40 kg a . i . / h a and f l u o r e s c e n c e curves c h a r a c t e r i s t i c of the v e r y r e s i s t a n t p l a n t s found i n i n f e s t e d corn f i e l d s (19). Thus, a change o f phenotype o c c u r s w i t h i n one g e n e r a t i o n a f t e r a c h e m i c a l s t i m u l u s . T h i s seems t o be one o f t h e v e r y few c a s e s o f e n v i r o n m e n t a l l y i n d u c e d g e n e t i c changes c i t e d i n the l i t e r a t u r e (37, 38). Up t o now, we have not f o u n d r e l e v a n t d i f f e r e n c e s o f growth, r e p r o d u c t i o n , psbA sequence, p h o t o c h e m i c a l c h a r a c t e r i s t i c s , i n v i t r o c h l o r o p l a s t r e s p o n s e t o a t r a z i n e and membrane l i p i d s (19, 39) between Type I mutants and i n d u c e d r e s i s t a n t mutants ( R i ) . C r o s s e s u s i n g S, I , R i , and t r e a t e d Type I mutants ( I i ) were s t u d i e d t o d e t e r m i n e the n a t u r e and t h e i n h e r i t a n c e o f the i n d u c t i o n . Prelimi n a r y r e s u l t s showed t h e p r e s e n c e o f I and R phenotypes a t the F generation of I x R crosses. Some e x c e p t i o n a l c r o s s e s w i t h p a t e r n a l i n h e r i t a n c e were s t u d i e d i n d e t a i l and showed p e c u l i a r f e a t u r e s i n subsequent F to F generations (40). 2

x

5

T h e r e f o r e , even w i t h an a p p a r e n t l y s i m p l e m a t e r n a l i n h e r i t a n c e , t h e gene f o r a t r a z i n e r e s i s t a n c e may be e x p r e s s e d i n d i f f e r e n t ways a c c o r d i n g t o t h e g e n e t i c background. SPREAD OF

RESISTANCES FROM CROPS

W i t h t h e r e l e a s e o f c r o p s , i n which f o r e i g n genes f o r a n t i b i o t i c o r h e r b i c i d e r e s i s t a n c e s ( e . g . , b a c t e r i a l genes) have been i n t r o d u c e d u s i n g recombinant DNA t e c h n i q u e s , the r i s k o f d i s p e r s a l o f f o r e i g n genes become a c t u a l . The p o s s i b l e s p r e a d o f such genes t h r o u g h i n s e r t i o n i n v i r u s e s , b a c t e r i a l , and nematodes t h a t l i v e i n c l o s e c o n t a c t w i t h t r a n s g e n i c p l a n t s s h o u l d be s t u d i e d . However, o u t c r o s s i n g w i t h r e l a t e d w i l d s p e c i e s s h o u l d be o f g r e a t e r c o n c e r n . O u t c r o s s i n g was known f o r a l o n g time under the t e r m i n o l o g y o f introgression. Intro^ressions: I n t r o g r e s s i o n o r o u t c r o s s i n g between c u l t i v a t e d and w i l d p l a n t s o f t e n r e s u l t s i n t h e r e l e a s e o f more a g g r e s s i v e weeds. Examples o f t h i s f e a t u r e can be found i n Raphanus ( 4 1 ) , S e c a l e ( 4 2 ) , Sorghum ( 4 3 ) , and S e t a r i a ( 4 4 ) . A good example o f i n t r o g r e s s i o n r e l a t e d t o weed c o n t r o l p r a c t i c e s was t h e use o f r e d pigmented r i c e i n I n d i a because i t made hand weeding o f w i l d p l a n t s e a s i e r . Ten y e a r s l a t e r , w i l d p l a n t s w i t h a p u r p l e c o l o r a t i o n i n t h e i r l e a v e s were f o u n d i n a weed p o p u l a t i o n ( 4 5 ) , t h u s i n d i c a t i n g h y b r i d i z a t i o n s between c u l t i v a t e d and w i l d r i c e . The p u r p l e c h a r a c t e r i s t i c would most l i k e l y s p r e a d i n weed p o p u l a t i o n s because i t e s c a p e d hand weeding.


24. DARMENCY AND GASQUEZ

Fate of Herbicide Resistance Genes in Weeds

S i m i l a r l y , one c a n a s k whether t h e d i c l o f o p - m e t h y l r e s i s t a n t w i l d o a t p o p u l a t i o n s i n A u s t r a l i a a r e t h e r e s u l t o f c r o s s e s between w i l d p l a n t s and some t o l e r a n t o a t c u l t i v a r . Indeed, an o a t c u l t i v a r t h a t has been shown t o be t o l e r a n t t o d i c l o f o p has been grown f o r 85 y e a r s . Because t h i s t r a i t a p p e a r e d t o be s i m p l y i n h e r i t e d (2 n u c l e a r l o c i ( 4 6 ) , t h e t r a n s f e r o f t o l e r a n t genes i n t o t h e w i l d o a t c o u l d have o c c u r r e d l o n g b e f o r e any h e r b i c i d e s p r a y .


The r i s k o f p a s s i n g r e s i s t a n c e genes from a c r o p t o a w i l d r e l a t e d species i s not inconceivable. A number o f c r o p s , ( e . g . , r i c e , m i l l e t s , sorghum, o a t s , r a p e s e e d , sugar b e e t s , s u n f l o w e r , a l f a l f a , p e a s , and p o t a t o e s ) c o u l d be i n v o l v e d i n i n t r o g r e s s i o n . Therefore, as h e r b i c i d e r e s i s t a n t c r o p s a r e e n g i n e e r e d , a g e n e t i c b a r r i e r between c r o p s and weeds must be d e v i s e d . L i m i t a t i o n o f t h e Spread: The s p r e a d o f genes from t r a n s g e n i c p l a n t s i s g e n e r a l l y i n t e r p r e t e d as r e s u l t i n g from p o l l e n d i s p e r s a l o f t h e c r o p toward w i l d p l a n t s . T h e r e f o r e , i t c o u l d be t h a t m a t e r n a l i n h e r i t a n c e o f a r e s i s t a n c e t r a i t , as f o r a t r a z i n e r e s i s t a n c e , may g r e a t l y d e l a y t h e time needed t o r e l e a s e r e s i s t a n t weeds. The gene f l u x between an a t r a z i n e r e s i s t a n t f o x t a i l m i l l e t ( S e t a r i a i t a l i c a ) and i t s w i l d r e l a t i v e , t h e g r e e n f o x t a i l (S. v i r i d i s ) i s now b e i n g i n v e s t i g a t e d . T r i a z i n e r e s i s t a n c e found i n one p l a n t o f t h e w i l d g r e e n f o x t a i l was t r a n s f e r r e d t o t h e c u l t i v a t e d f o x t a i l m i l l e t t o improve weed c o n t r o l i n t h i s crop (47). Growing f o x t a i l m i l l e t w i t h a t r a z i n e r e s i s t a n t c y t o p l a s m i n a r e a s i n f e s t e d w i t h g r e e n f o x t a i l may r e s u l t i n t h e f e r t i l i z a t i o n o f some f l o r e t s o f c u l t i v a t e d s p i k e s by p o l l e n from w i l d p l a n t s . This i s l i k e l y t o occur c l o s e t o the border o f a f i e l d , where w i l d p l a n t s grow, as w e l l as w i t h i n a f i e l d where some p l a n t s s u r v i v e d h e r b i c i d e a p p l i c a t i o n s . Spontaneous h y b r i d i z a t i o n s l e a d t o l e s s t h a n 0.01% h y b r i d s o f t h e c r o p ( u n p u b l i s h e d d a t a ) , and n e a r l y 0.2% o f t h e w i l d p l a n t s ( 4 5 ) . Because h a r v e s t machines l e a v e a s m a l l p r o p o r t i o n o f g r a i n on t h e s o i l and f o x t a i l m i l l e t y i e l d i s more t h a n 1 0 g r a i n s / h a , i t i s h i g h l y p r o b a b l e t h a t r e s i s t a n t h y b r i d seeds w i l l be r e l e a s e d i n t h e soil. 9

The b e h a v i o r o f h y b r i d p l a n t s and t h e i r d e s c e n d e n t s w i l l depend on s e e d v i a b i l i t y , p r e d a t i o n and g e r m i n t i o n , p l a n t s u r v i v a l from h e r b i c i d e o r c r o p c o m p e t i t i o n , f e r t i l i t y , and gene exchanges w i t h i n the weed p o p u l a t i o n . P r e l i m i n a r y e s t i m a t e s l e a d us t o t h i n k t h a t the r i s k o f h a v i n g r e s i s t a n t weeds i s n o t a c c e p t a b l e . Therefore, i t i s n e c e s s a r y t o s t a r t a b r e e d i n g program t o produce a t e t r a p l o i d r e s i s t a n t f o x t a i l m i l l e t t h a t r e d u c e s t h e chance o f h a v i n g v i a b l e h y b r i d s between t h e c r o p and t h e weed. CONCLUSION S e v e r a l a s p e c t s o f t h e appearance o f r e s i s t a n c e genes and p l a n t s i n weed p o p u l a t i o n s were i l l u s t r a t e d u s i n g d a t a from t r i a z i n e resistance studies. The f o l l o w i n g a p p l i e s t o weeds r e s i s t a n t t o t r i a z i n e s ; some p e c u l i a r genomes a p p e a r e d t o be a b l e t o p r o d u c e a h i g h number o f mutants and, t h e r e f o r e , mutants do n o t appear a t random i n f i e l d s ; t h i s r e s u l t s i n a f o u n d e r e f f e c t i n e a c h r e s i s t a n t p o p u l a t i o n ; t h e p r e s e n c e o f t h e mutated c h l o r o p l a s t gene i s n o t s u f f i c i e n t t o b r i n g about h i g h l y r e s i s t a n t p l a n t s ; s p r e a d o f t h e r e s i s t a n c e genes from e n g i n e e r e d c r o p p l a n t s t o w i l d p l a n t s i s l i k e l y t o occur i n s p i t e o f a cytoplasmic i n h e r i t a n c e .


36

362

MANAGING

RESISTANCE TO AGROCHEMICALS


These c h a r a c t e r i s t i c s a r e p e c u l i a r t o t r i a z i n e r e s i s t a n c e , b u t t h i s example may be a good s t u d y model. T h i s s t u d y r e v e a l e d bottlenecks t h a t have r e d u c e d t h e s p r e a d o f t r i a z i n e r e s i s t a n t p l a n t s . It will be i m p o r t a n t t o d i s c o v e r and a n a l y z e s i m i l a r phenomena i n f u t u r e cases o f h e r b i c i d e r e s i s t a n c e (48). T h i s knowledge w i l l be h e l p f u l i n e l a b o r a t i n g m a t h e m a t i c a l models and d e t e r m i n i n g weed c o n t r o l s t r a t e g i e s t o p r e v e n t h e r b i c i d e r e s i s t a n t p l a n t s from a p p e a r i n g and spreading. However, e a c h new r e s i s t a n c e t h a t d e v e l o p s w i l l p r o d u c e a d i f f e r e n t g e n e t i c s i t u a t i o n . The s o l u t i o n s f o u n d b y weeds t o escape h e r b i c i d e s e l e c t i o n p r e s s u r e s may be v a r i e d . Due t o t h e h i g h s e l e c t i v e v a l u e c o n f e r r e d b y t h e r e s i s t a n c e genes i n h e r b i c i d e t r e a t e d a r e a s , m u t a t i o n e v e n t s a t v e r y low f r e q u e n c i e s have h i g h p r o b a b i l i t y t o l e a d t o t h e appearance o f r e s i s t a n t p l a n t s . I n a d d i t i o n , weeds w i l l c e r t a i n l y d i s p l a y a f t e r a s h o r t d e l a y t h e b a c t e r i a l genes t r a n s f e r r e d t o c r o p s f o r h e r b i c i d e r e s i s t a n c e , and some w i l d p l a n t s c o u l d be e x p e c t e d t o become new weeds because o f r e s i s t a n t genes.

LITERATURE CITED 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13. 14. 15. 16. 17. 18. 19. 20. 21. 22. 23. 24.

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Fate of Herbicide Resistance Genes in Weeds - ACS Symposium

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