Chemical Modification of Plant Response to Temperature Extremes

19 Chemical Modification of Plant Response to Temperature Extremes M E R Y L N. CHRISTIANSEN and J U D I T H B. ST. J O H N

Downloaded by UNIV LAVAL on July 14, 2016 | http://pubs.acs.org Publication Date: July 6, 1984 | doi: 10.1021/bk-1984-0257.ch019

Agricultural Research Service, U.S. Department of Agriculture, Beltsville, M D 20705

Lipid synthesis in vegetative tissue can be modified by pyridazinones. The major effect is blockage of desaturation of linoleic acid to linolenic acid. The blockage of linolenic acid synthesis inhibits cold hardening and increases chilling sensitivity of cotton and freezing susceptibility of winter grains. Other modifications of lipid synthesis include an increase in leaf cuticular wax up to 55%. Foliar wax increase improves water economy of soybean, corn, sorghum and cotton.

Temperature is the primary environmental factor that l i m i t s where and how successfully a g r i c u l t u r a l crops can be grown. There is a wide range of genetic d i v e r s i t y among economic crop species in a b i l i t y to tolerate temperature extremes. Many t r o p i c a l species are injured by temperatures above 0°C., while temperate zone species can withstand temperatures as low as -70°C. An understanding of the nature of low temperature resistance or of c h i l l i n g and freezing injury is e s s e n t i a l l y lacking. Various studies have associated membrane form and function with low temperature r e l a t i o n s . A v a r i e t y of physiological dysfunctions of c h i l l e d and frozen plants have been related to membrane perturbation ( 1) . Many of the changes induced by low temperature are characterized by changes in l i p i d s . The changes may be an a l t e r a t i o n of classes such as an increase in t o t a l polar l i p i d , or of t r i g l y c e r i d e s or only an a l t e r a t i o n of constituent fatty acids. A declining temperature is almost u n i v e r s a l l y e f f e c t i v e in increasing fatty acid unsaturation. Reduction in oleate and l i n o l e a t e and an increase in linolenate is usual in winter hardening plants (2,). An increase in functionality of c e l l s at low temperature may be concurrent with increased fatty acid unsaturation . Processes such as water transport, respiration, and photosynthesis in hardened tissue are less inhibited by low temperatures. The function of membranes is requisite for osmotic control of cell This chapter not subject to U.S. copyright Published 1984, American Chemical Society

Ory and Rittig; Bioregulators ACS Symposium Series; American Chemical Society: Washington, DC, 1984.


236

BIOREGULATORS: CHEMISTRY AND USES

contents and of water. Resistance to chilling, frost, and freezing is dependent upon a membrane-regulated orderly dehydration of c e l l s with a concurrent rise in cell osmotic concentration. Chemical r e g u l a t i o n of f a t t y a c i d should, t h e r e f o r e , p r o v i d e a tool to m a n i p u l a t e p l a n t response to t e m p e r a t u r e . Such an a b i l i t y to r e g u l a t e p l a n t response to temperature would o b v i o u s l y be u s e f u l to abate c o l d and h e a t damage to c r o p p l a n t s . I t would l i k e w i s e be u s e f u l to c o n t r o l unwanted v e g e t a t i o n (weeds) by i n d u c i n g g r e a t e r s u s c e p t i b i l i t y to heat or c o l d . There is little p a s t h i s t o r y c o n c e r n i n g the use o f c h e m i c a l s to a l t e r l i p i d s in p l a n t s . A l t e r a t i o n of f a t t y acid composition of micro-organisms by selective fatty acid supplements has provided evidence t h a t temperature response can be altered by changes in l i p i d components. McElhaney (3) showed t h a t treatment of A s p e r g i l l i s l a i d l a w i i w i t h f a t t y a c i d supplements s h i f t e d the membrane phase transition to a different temperature level. Membrane l i p i d a l t e r a t i o n as a r e s u l t o f temperature a c c l i m a t i o n is common in p l a n t s , animals and m i c r o o r g a n i s m s and has been r e l a t e d t o f l u i d i t y o f membranes a t low temperature in Tetrahymena pyriformis (4,5). In these s t u d i e s the a c t i v i t i e s o f membrane bound f a t t y a c i d d e s a t u r a s e s were c o n t r o l l e d by membrane f l u i d i t y at low temperature. Fatty acid composition of membrane p h o s p h o l i p i d s can r e f l e c t the l i p i d c o m p o s i t i o n o f the c u l t u r e o r d i e t ; e.g. a n i m a l s fed c o r n o i l (6,), y e a s t grown in media o f d i v e r s e f a t t y a c i d s (1); or p o t a t o t u b e r t i s s u e i n c u b a t e d in media of v a r y i n g f a t t y a c i d u n s a t u r a t i o n or c h a i n l e n g t h (7). Treatment of tomato ( L y c o p e r s i c u m e s c u l e n t i u m ) w i t h e t h a n o l a m i n e - t w e e n oleate altered phospholipid composition and reduced chilling i n j u r y symptoms (8). C o n s i d e r a b l e c o n t r o v e r s y has p r e v a i l e d over the i n t e r r e l a t i o n of membrane f a t t y a c i d u n s a t u r a t i o n , membrane f l u i d i t y at low temperature and p l a n t r e s i s t a n c e to c h i l l i n g or freezing (1). Some r e s e a r c h e r s (2,) h o l d t h a t t h e r e is no r e l a t i o n between l i p i d u n s a t u r a t i o n and p l a n t s u r v i v a l a t low t e m p e r a t u r e . They c i t e as evidence the l a c k o f d i f f e r e n c e s in l i p i d u n s a t u r a t i o n between freeze hardy and unhardy wheat varieties. Other researchers suggest a u n i v e r s a l need f o r u n s a t u r a t e d l i p i d s in membranes to insure fluidity and hence functionality at low temperature. Unless f l u i d i t y and consequent f u n c t i o n a l i t y e x i s t s , subsequent c o l d h a r d e n i n g e v e n t s cannot o c c u r (9). Pyridazinone compounds were first reported to alter p r o d u c t i o n o f p o l a r l i p i d s o f c h l o r o p l a s t s ( 1() ). In subsequent work, S t . John ( L I ) i d e n t i f i e d p y r i d a z i n o n e s that specifically i n h i b i t e d p r o d u c t i o n in v e g e t a t i v e t i s s u e o f l i n o l e n i c a c i d w i t h c o n c u r r e n t i n c r e a s e s in l i n o l e i c a c i d . The p y r i d a z i n o n e s appeared to be e x c e l l e n t t o o l s t o s e t t l e the d i s p u t e over the s i g n i f i c a n c e of f a t t y a c i d u n s a t u r a t i o n in the c o l d h a r d e n i n g p r o c e s s . The i n i t i a l e x p e r i m e n t s were concerned w i t h c h i l l i n g injury to s e e d l i n g c o t t o n . C h i l l i n g i n j u r y in c o t t o n s e e d l i n g s is caused by c o l d inactivation o f r o o t water uptake; the p l a n t suffers dehydration (12). Cotton s e e d l i n g s can be chill hardened to t o l e r a t e 5-8°C. by g r a d u a l l y l o w e r i n g the temperature from 20° to 8°. The q u e s t i o n s we posed were: (1) Does l i n o l e n i c acid


19. CHRISTIANSEN AND ST. JOHN

237

Temperature Extremes


i n c r e a s e in c o t t o n r o o t s w i t h r e d u c t i o n in temperature? (2) W i l l the p y r i d a z i n o n e s b l o c k a low temperature i n d u c e d i n c r e a s e in l i n o l e n i c acid? ( 3 ) I f l i n o l e n i c a c i d s y n t h e s i s is b l o c k e d will the r e s p o n s e t o low temperatures be a l t e r e d in terms o f s e n s i t i v i t y t o c h i l l i n g and a b i l i t y t o harden? Seeds were g e r m i n a t e d a t temperatures o f 15, 20, 25 and 3 0 ° in paper rolls wet with either water or BASF 13338, [4-chloro-5(dimethyamino-2 phenyl-3 ( 2 H ) - p y r i d a z i n o n e ] a t 10 um concentration. Seeds were germinated 24 h o u r s a t 3 0 ° , 40 hours at 25, 70 hours a t 2 0 ° and 168 hours a t 15°C. t o i n s u r e e q u a l l y sized seedlings. Root t i p (1 cm) and h y p o c o t y l (2 cm) were collected and f r e e z e dried for lipid analysis as p r e v i o u s l y d e s c r i b e d (13). E f f e c t s o f temperature and BASF 13338 t r e a t m e n t on s e e d l i n g growth were determined on seeds g e r m i n a t e d a t 3 0 ° , c u l t u r e d in growth chambers and t r e a t e d w i t h water o r 20 uM BASF 13338 in the c u l t u r e media [5 ug/g (w/w) ] . S e e d l i n g s were c h i l l hardened by g r a d u a l l y l o w e r i n g temperature (5°/48 h r ) to 15°. A c o n t r o l and BASF 13338 t r e a t m e n t were n o t hardened b u t grown 8 days at 30°. After t h e above temperature sequences, a l l t r e a t m e n t s were c h i l l e d 4 days a t 8 ° , then grown f o r seven days in the greenhouse t o d e t e r m i n e s u r v i v a l and i n j u r y symptoms. The f a t t y a c i d s o f the p o l a r l i p i d s o f t h e r o o t t i p s were p r o g r e s s i v e l y h i g h e r in l i n o l e n i c a c i d as growth temperature was reduced ( T a b l e I ) . BASF 13338 e s s e n t i a l l y b l o c k e d low temperature induction of linolenic acid synthesis and caused a c o n c u r r e n t i n c r e a s e in l i n o l e i c acid. S e e d l i n g s w i t h reduced levels of membrane-bound l i n o l e n i c a c i d were l e s s a b l e t o s u r v i v e c h i l l i n g temperature and s u r v i v i n g s e e d l i n g s were abnormal ( T a b l e I I ) ( 1 3 ) .

Table I .

Fatty Acid

C o m p o s i t i o n o f P o l a r L i p i d s o f 1-cm o f C o t t o n S e e d l i n g R a d i c l e s (13)

Foot T i p s

Growth Temperature °C.

16:0

F a t t y A c i d (%) 18:2 18:1 18:0

18:3

Control (water)

30 25 20 15

32.6 35.3 32.9 31.6

3.7 2.8 3.3 4.8

7.5 5.7 5.4 4.2

36.3 33.4 31.7 31.9

13.6 22.9 26.8 27.5

BASF 13338 (10 uM)

30 25 20 15

34.7 34.4 34.5 30.9

2.8 2.7 3.7 4.1

7.6 5.7 6.4 4.6

44.0 43.1 41.7 43.7

10.9 14.0 13.7 17.1

Treatment


238


Table I I .

Cotton Seedling Survival 7 Days a f t e r 96 Hr of C h i l l i n g at 8°C. (13)

Seedling C l a s s i f i c a t i o n Normal Abnormal Dead % Control 30°C., 8 days 62 3 35 BASF 13338 (10 uM) 30°C., 8 days 60 40 0 Control, hardened 92 0 9 BASF 13338 (10 uM), hardened 20 80 0 Seedlings with 50% of cotyledon necrotic were classed abnormal. Grown 2 days at 30°C., 2 days at 25°C., 2 days at 20°C., and 2 days at 15°C. Growth Conditions

1

2


2

After ascertaining an association between l i n o l e n i c acid and chilling sensitivity in cotton, research to determine the e s s e n t i a l i t y of linolenate to freeze hardening in winter grains was i n i t i a t e d . Willemot (14) reported that both the accumulation of l i n o l e n i c acid and development of freezing tolerance were inhibited when wheat seedlings were treated with BASF 13338 t h i r t y - s i x hours before frost hardening. These findings were extended into a f i e l d s i t u a t i o n (15). BASF 13338 was soil incorporated at seedling time at rates of 0, 2.8, 5.2 and 11.2 kg/ha. Wheat (Triticum aestivum L. cvs. Arthur and Potomac), barley Hordeum vulgare L., and rye (Secale céréale L.) were sown in the f a l l . V i s u a l evidence of cold injury of BASF 13338 treated plants became evident after the f i r s t f r o s t . Severity of cold injury increased with increased rate of BASF 13338 a p p l i c a t i o n . Fatty acid composition of membrane l i p i d s from seedling shoots of BASF 13338 treated plants had s i g n i f i c a n t l y lower levels of l i n o l e n i c acid (Table I I I ) . Reduced l e v e l of l i n o l e n i c acid was d i r e c t l y related to reduced plant survival (Table IV) and reduced t i l l e r i n g of surviving plants (Table V). There was evidence of v a r i e t a l and genus differences in s e n s i t i v i t y to BASF 13338. The decreasing order of s e n s i t i v i t y was Authur, Potomac wheats, Monroe barley and Abruzzi rye. The data indicate a r e l a t i o n between l i n o l e n i c acid and winter survival of cereals. Other evidence suggests that in winter cereals, l i n o l e n i c acid is not the l i m i t i n g factor in the minimal temperature tolerated. De La Roche (2) has suggested that i t is the i n h i b i t i o n of photosynthesis by pyridazinones (10) that is responsible for increased cold s e n s i t i v i t y . However, other pyridazinones inhibit photosynthesis (Pyrazon); but do not a f f e c t l i n o l e n i c acid or reduce cold hardening of winter wheat. Also, pyridazinones reduce l i n o l e n i c acid levels in non-photosynthetic tissues (13).


Table I I I .

Effect of Preemergence Treatment with BASF 13338 on Membrane Fatty Acid Composition of Shoot Tissue from Small Grains (15) BASF 13338 kg/ha O.0 2.8 5.6 11.2

10.1 8.8 8.4 8.7

a b b b

O.8 a O.8 a O.6 a O.8 a

1.8 2.4 2.1 2.2

a a a a

11.7 35.4 50.0 61.4

a b c d

75.6 52.8 38.9 27.1

a b c d

Potomac wheat

O.0 2.8 5.6 11.2

10.0 9.1 8.8 9.4

a a a a

1.1 1.0 1.0 1.2

a a a a

1.9 2.6 2.3 2.4

a a a a

11.7 35.4 44.0 54.5

a b c d

75.4 52.4 44.0 32.5

a b c d

Monroe barley

O.0 2.8 5.6 11.2

11.6 10.0 10.4 10.4

a b ab ab

1.3 1.0 1.2 1.3

a a a a

1.7 1.4 1.7 1.5

a a a a

10.0 20.8 31.9 40.2

a b c d

75.4 66.9 54.9 46.6

a b c d

Species Arthur wheat


239



Fatty acid compo e i t i o n by weight 16:0 18:0 18:1 18:2

1

(%) 18:3

Abruzzi rye

O.0 14.2 a 11.3 a 2.4 a 1.0 a 2.8 2.1 a 18.4 b 10.2 ab O.8 a 5.6 9.8 bc 32.4 c 2.4 a O.9 a 11.2 30.8 c 8.8 c 1.7 a O.9 a Values for individual fatty acids within a cereal followed common l e t t e r s are not s i g n i f i c a n t l y d i f f e r e n t at the 5% with Duncan's Multiple Range Test.

71.3 a 65.7 b 54.5 c 57.6 c by level

Table IV. Effect of BASF 13338 on the survival of winter cereals following a freeze at -5°C. (15)

Species

Arthur wheat

Control

S u r v i v i a l (%) BASF 13338 (10 ug/g)

96

29

Potomac wheat

100

0

Monroe barley

93

0

Abruzzi rye

93

0



240

T a b l e V.

E f f e c t o f BASF 13338 A p p l i e d Preemergence on T i l l e r i n g of W i n t e r C e r e a l s D u r i n g W i n t e r o f 1977-78 (15) BASF 13338 (kg/ha) 5.6 2.8 —Mean no. o f t i l l e r s / m o f row—

Species 0

224

al

174

b

124

c

11 d

Potomac wheat

183

a

173

a

60

b

5 c

Monroe b a r l e y

164

a

138

a

60

b

3 c

Abruzzi

199

a

133

b

99

b

9 c

Arthur


11.2

wheat

rye

V a l u e s f o l l o w e d by common l e t t e r s are not s i g n i f i c a n t l y d i f f e r e n t at the 5% l e v e l w i t h Duncan's M u l t i p l e Range T e s t .

Treatment with BASF 13338 reduced the proportions of linolenic acid in phosphatidylcholine (Table VI) phosphatidylathanolamine, and the t o t a l p o l a r l i p i d s of c e r e a l roots at a l l growth temperatures (16,. The distribution of phospholipid classes was not influenced by temperature or treatment w i t h BASF 13338 ( T a b l e V I I ) . Proportions of l i n o l e n i c a c i d in r o o t membranes were not r e l a t e d to the r a t e o f r e s p i r a t i o n from 4 t o 30C, the a c t i v a t i o n e n e r g i e s o f r e s p i r a t i o n , or the temperature at which the change in activation occurred. P r o p o r t i o n s o f l i n o l e n i c a c i d in r o o t membranes o f c e r e a l s may limit other membrane-associated processes such as active t r a n s p o r t , water and i o n p e r m e a b i l i t y , and membrane r e s i l i e n c e .

These c o l l e c t i v e s t u d i e s i n d i c a t e d that the pyridazinones a l t e r the r e s p o n s e o f c o t t o n and c e r e a l s t o low t e m p e r a t u r e s . We c o n j e c t u r e d t h a t the p y r i d a z i n o n e s might a l s o a l t e r the r e s p o n s e o f some p l a n t s p e c i e s to h i g h temperatures. Field tests with S i l v e r Queen c o r n i n d i c a t e d t h a t preemergence treatment w i t h BASF 13338 a m e l i o r a t e d h i g h temperature s t r e s s , p r o b a b l y by a l t e r n a t i o n o f water s t a t u s (17). Growth chamber s t u d i e s were conducted on the heat t o l e r a n c e o f c o r n (Zea mays L.) and sorghum [Sorghum bicolor (L.) Moench]. Corn and sorghum p l a n t s were grown at 30°C. and t r a n s f e r r e d to 40°C. P l a n t s t r e a t e d w i t h BASF 13338 transpired significantly (P = O.01) l e s s water than untreated controls at 40°C.; the measured rates were O.59 g H2O; cm leaf area/24 hr and O.72 g R,O/cm leaf area/24 hr, respectively. Soybean and c o t t o n p l a n t s t r e a t e d w i t h BASF 13338 t r a n s p i r e d 20-30% l e s s water than c o n t r o l p l a n t s ( T a b l e V I I I ) . The d i f f e r e n c e in water l o s s d i d not seem t o i n v o l v e stomates since there were no differences in diffusive resistance or pressure bomb r e a d i n g s between c o n t r o l and BASF 13338 t r e a t e d leaves. Furthermore, internal l e a v e water content, determined g r a v i m e t r i c a l l y , d i d not d i f f e r between l e a v e s o f c o n t r o l and t r e a t e d p l a n t s . P y r i d a z i n o n e - i n d u c e d i n c r e a s e s in c u t i c u l a r waxes 2

2



241


may e x p l a i n the a l t e r a t i o n s in water s t a t u s . The c u t i c u l a r wax o f soybeans grown in the greenhouse in n u t r i e n t s o l u t i o n s c o n t a i n i n g 15 ppm BASF 13338 were increased 40% over control levels. P y r i d a z i n o n e t r e a t m e n t i n c r e a s e d c u t i c u l a r waxes o f soybean l e a v e s by as much as 55% under f i e l d c o n d i t i o n s ( T a b l e I X ) . Thus the e v i d e n c e seems t o i n d i c a t e t h a t BASF 13338 does a l t e r the water economy o f p l a n t s , p r o b a b l y t h r o u g h e f f e c t s on wax d e p o s i t i o n on l e a v e s and c u t i c u l a r water r e l a t i o n s .

Table V I .


Treatment

Control

BASF 13338 (100 uM)

F a t t y A c i d Composition o f Phosphatid y l Choline Roots o f Wheat S e e d l i n g s (16) Growth Temperature °C.

16:0

18:0

from

Fatty Acid 18:1 18:2 % by weight

18:3

25

27

2

5

49

16

20

22

3

10

44

21

15

26

5

9

34

26

10

24

2

6

32

36

25

25

2

5

63

5

20

23

3

7

61

5

15

21

4

58

7

9

10 63 11 19 2 5 P h o s p h o l i p i d s were s e p a r a t e d u s i n g h i g h performance l i q u i d chromat o g r a p h y . The p h o s p h a t i d y l c h o l i n e f r a c t i o n was c o l l e c t e d and the f a t t y a c i d composition determined.

Chemical modification of plant temperature r e l a t i o n s are p o s s i b l e through a l t e r a t i o n o f p o l a r l i p i d s o f membranes. Use o f pyridazinone to i n h i b i t f a t t y a c i d desaturases r e s u l t s in lower levels of linolenic a c i d in p o l a r lipids and a concurrent r e d u c t i o n o f p l a n t t o l e r a n c e t o c h i l l i n g in t r o p i c a l s p e c i e s and f r e e z i n g in w i n t e r g r a i n c r o p s . A l t e r a t i o n in l i p i d s a l s o c o n f e r s t o l e r a n c e t o "summer s t r e s s " and improved water economy which c a n be a t t r i b u t e d t o i n c r e a s e s in l e a f c u t i c u l a r wax which r e d u c e s cuticular transpiration.


242


Table V I I .

Phospholipid

Treatment


Control

BASF 13338 (100 uM)

C o m p o s i t i o n o f Whea t S e e d l i n g

Roots (16)

Growth Temperature °C.

PE

25

34

20

37

5

4

6

48

15

31

8

7

3

52

10

38

6

7

4

45

25

35

6

5

4

50

20

33

6

5

2

54

15

34

5

7

4

50

2

Phosph o l i p i d F r a c t i o n s PA-PS PG PI % l i p i d phosp orus 7 4 5

1

PC 51

10 37 5 4 3 51 P h o s p h o l i p i d s were s e p a r a t e d i n t o f i v e f r a c t i o n s u s i n g h i g h performance l i q u i d chromatography. F r a c t i o n s were c o l l e c t e d and the phosphorus c o n t e n t determined by B a r t l e t t ' s m o d i f i c a t i o n o f the Fiske-Subbarow method (18) PE = p h o s p h a t i d y l e t h a n s t a m i n e , PG - p h o s p h a t i d y l g l y c e r o l ; PI = p h o s p h a t i d y l i n o s i t o l ; PA-PS = p h o s p h a t i d i c a c i d + p h o s p h a t i d y l s e r i n e ; PC = p h o s p h a t i d y l s e r i n e .

Table V I I I .

Effect

o f BASF 13338 on Water L e s s by and Soybean a t 30°C.

Treatment 15 ppm BASF 13338 in Nutrient Solution

Cotton

Water Use % of Control (Cotton)

72

15 ppm BASF 13338 in N u t r i e n t S o l u t i o n (Soybean)

78

S o i l - BASF 13338 - 50 mg/kg (Soybean)

76


19.

T a b l e IX. E f f e c t


Literature

4. 5. 6. 7. 8. 9.

10. 11. 12. 13. 14. 15. 16. 17.

18.

243

o f BASF 13338 on C u t i c u l a r Wax o f F i e l d C u l t u r e d C l a r k Soybean

BASF 13338 Rate kg/ha 0

1. 2. 3.


CHRISTIANSEN A N D ST. J O H N

L e a f Wax ug/cm L e a f 2

% Increases

(%)

4.79

5

5.29

12

10

7.43

55

Cited

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February 22, 1984


Chemical Modification of Plant Response to Temperature Extremes

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