Influence of Exogenous Zearalenone on Plant Generative Development

For agriculture plants, effective flowering is a very important process. In this process, a vegetative meristem changes into a reproductive meristem which is capable of forming floral organs and in this way completes the reproductive life cycle of higher plants (Bernier and Perillex 2005). How the vegetative meristem is able to perceive and interpret signals from the environment as well as from the plant itself is largely unknown. The process by which vernalization - the exposure of a germinating seed or a juvenile plant to a prolonged period of low temperature - promotes flowering in an adult plant has remained a mystery for many years (Michales and Amasimo 2000). Vernalization is an important control for many agricultural and horticultural production species in temperate regions.

Some studies indicated that exogenous zearalenone influences plant growth and development. For example, zearalenone stimulated the initiation of the vegetative bud in tobacco pith callus tissue (Mirocha et al. 1968), inhibited the cell membrane transport of maize roots (Vianello and Macri 1981) and enhanced the a-amylase and b-glucosidase activities of germinating maize seeds.

Meng et al. (1992) found that zearalenone was an endogenous regulator controlling induction of generative development in winter plant. An increase in endogenous zearalenone during vernalization was also recorded by Fu and Meng (1994) in many winter plants. Moreover, they suggested that exogenous zearalenone can partly replace the low temperature requirement for flowering in winter wheat.

In combination with greatly shortened vernalization (14 days, 5°C) zearalenone completely eliminated the flowering blockade of winter wheat cv. Grana, which usually requires vernalization of 8-9 weeks (Biesaga-Koscielniak 1998) (Table 15.1). Moreover, zearalenone in the concentration 2 mg/dm3 reduced the length of the vegetative phase by as much as about 50 days in comparison with the control sample (Biesaga-Koscielniak 2001) (Fig. 15.2). The stimulating effect of zearalenone on the induction of heading was observed also in other wheat varieties, and its effectiveness was highest in those varieties which needed longer time of low temperature treatment to flowering induction (Table 15.2). Some zearalenone derivatives exercised a greater influence on the induction of heading and the rate of generative development

Table 15.1 The influence of zearalenone on the generative development of winter wheat cv. 'Grana' after various periods of vernalization (According to Biesaga-Koscielniak 1998, modified). Isolated wheat embryos were cultured in sterile conditions on Murashige and Skoog (1962) media supplemented with 0 (control), 0.25, 0.50, 0.75 and 2.00 mg/dm3 of zearalenone during 14, 28 and 42 days at 5°C (vernalization). After these periods, plants were transferred to soil and cultivated at 20/17°C. Number of headed plants, generative development of apexes and number of vegetative ones was obtained after 100 days of grown at 20/17°C

Number of plants

Table 15.1 The influence of zearalenone on the generative development of winter wheat cv. 'Grana' after various periods of vernalization (According to Biesaga-Koscielniak 1998, modified). Isolated wheat embryos were cultured in sterile conditions on Murashige and Skoog (1962) media supplemented with 0 (control), 0.25, 0.50, 0.75 and 2.00 mg/dm3 of zearalenone during 14, 28 and 42 days at 5°C (vernalization). After these periods, plants were transferred to soil and cultivated at 20/17°C. Number of headed plants, generative development of apexes and number of vegetative ones was obtained after 100 days of grown at 20/17°C

Number of plants

Concentration of

Generative

Differentiation of frequency

zearalenone (mg/dm3)

Headed

(non-headed)

Vegetative

with respect to control

14 days of vernalization

0.25

57 (95)a

3

0

+

0.50

13 (22)

47

0

+

0.75

57 (95)

3

0

+

2.00

60 (100)

0

0

+

0.00 (Control)

13 (22)

14

33

28 days of vernalization

0.25

59 (98)

1

0

+

0.50

57 (95)

3

0

+

0.75

60 (100)

0

0

+

2.00

60 (100)

0

0

+

0.00 (Control)

35 (58)

25

0

42 days of vernalization

0.25

59 (98)

1

0

0.50

60 (100)

0

0

0.75

60 (100)

0

0

2.00

60 (100)

0

0

0.00 (Control)

49 (83)

10

0

'+'Significant differentiation on the basis of %2(p < test aIn brackets percent of headed plants in population

'+'Significant differentiation on the basis of %2(p < test aIn brackets percent of headed plants in population of winter wheat cv. Grana than this substance itself (Table 15.3). Very strong activity has been demonstrated, in particular, by a-zearalanol, which after only 7 days of vernalization at 5°C induced the heading of almost all plants and greatly reduced the duration of the vegetative phase. The effectiveness of zearalenone was increased by an addition of spermidine and tissue extracts from inflorescences of some plant species. The effect of zearalenone on the growth process of wheat was to some extent contrary to its effect on the generative development, since it inhibited the elongation of the shoots, and also reduced their ability to accumulate biomass. The role of zearalenone in inducing flowering of winter wheat plants was confirmed by experiments with an exogenous application of a zearalenone synthesis inhibitor (malathion). This inhibitor decreased the plants' heading ability even after long vernalization (Table 15.4).

The influence of zearalenone on the generative development of winter rape was much weaker in comparison with that of wheat. None of the concentrations which stimulated wheat plants induced the flowering of rape plants. Zearalenone treatment stimulated only the first step of the process of the shoot apices generative differentiation (Biesaga-Koscielniak 2001).

Concentration of zearalenone [mg x dm 3]

Fig. 15.2 The influence of zearalenone on the length of the phase from vernalization to flowering. Isolated embryos of winter wheat cv. 'Grana' were cultured in sterile conditions on Murashige and Skoog (1962) media supplemented with 0, 0.25, 0.50, 0.75 and 2.00 mg/dm3 of zearalenone during 14, 28 and 42 days at 5°C (vernalization). After vernalization seedlings were transferred to soil and cultured at 20/17°C (day/night) to flowering. For particular length of vernalization values marked with the same letter do not differ significantly according to Duncan's multiple range test (p < 0.05). For all investigated periods of vernalization, the best effect, observed as significant shortening of the length of the period between vernalization and flowering was noticed for 2 mg/ dm3 of zearalenone

Table 15.2 The influence of zearalenone on the generative development of nine winter wheat varieties. Isolated wheat embryos were cultured in sterile conditions on Murashige and Skoog (1962) media supplemented with 0 (control) and 2.00 mg/dm3 of zearalenone during 14 days at 5°C (vernalization). After this period, plants were transferred to soil and cultivated at 20/17°C. The number of heading and vegetative plants was fixed after 100 days from vernalization. The length of the phase from vernalization to flowering was determined in days

Table 15.2 The influence of zearalenone on the generative development of nine winter wheat varieties. Isolated wheat embryos were cultured in sterile conditions on Murashige and Skoog (1962) media supplemented with 0 (control) and 2.00 mg/dm3 of zearalenone during 14 days at 5°C (vernalization). After this period, plants were transferred to soil and cultivated at 20/17°C. The number of heading and vegetative plants was fixed after 100 days from vernalization. The length of the phase from vernalization to flowering was determined in days

Variety

Number of plants Control

Zearalenone

Differentiation of frequency with respect to control

Length of the phase from vernalization to flowering (days)

Headed

Vegetative

Headed

Vegetative

Control

Zearalenone

Kaja

45 (90)a

5

44 (88)

6

62

55

Almari

40 (80)

10

39 (85)

7

75

77

Tercja

40 (80)

10

44 (83)

9

75

70

Maltanka

17 (35)

31

21 (42)

29

71

69

Wanda

18 (35)

33

25 (50)

25

81

82

Jubilatka

13 (26)

37

33 (65)

18

+

79

67*

Kamila

12 (25)

36

30 (60)

20

+

85

61*

Zorza

5 (10)

45

44 (83)

9

+

99

71*

Izolda

5 (10)

45

39 (85)

7

+

89

73*

'+' Significant differentiation on the basis of %2(p < test aIn brackets percent of headed plants in population

'+' Significant differentiation on the basis of %2(p < test aIn brackets percent of headed plants in population

Table 15.3 Generative development of winter wheat plants after treatment with derivatives of zearalenone (According to Biesaga-Koscielniak 1998, modified). Seeds of wheat cv. 'Grana' were cultured in sterile conditions on Murashige and Skoog (1962) media supplemented with zearalenone and its derivative solutions used in concentration 2 mg/dm3 during 7 days at 5°C (vernalization). After vernalization plants were replaced to soil and cultured at 20/17°C. The number of heated and vegetative plants was fixed after 100 days of growth at 20/17°C, and for generative plants, the length of phase from vernalization to flowering was determined

Table 15.3 Generative development of winter wheat plants after treatment with derivatives of zearalenone (According to Biesaga-Koscielniak 1998, modified). Seeds of wheat cv. 'Grana' were cultured in sterile conditions on Murashige and Skoog (1962) media supplemented with zearalenone and its derivative solutions used in concentration 2 mg/dm3 during 7 days at 5°C (vernalization). After vernalization plants were replaced to soil and cultured at 20/17°C. The number of heated and vegetative plants was fixed after 100 days of growth at 20/17°C, and for generative plants, the length of phase from vernalization to flowering was determined

Zearalenopne derivatives

Number of plants

Length of phase from vernalization to flowering (days)

Headed

Vegetative

Differentiation of frequency with respect to zearalenone

a-Zearalenol

30 (60)a

20

63 ab

ß-Zearalenol

15 (30)

35

69 ab

Zearalanon

17 (35)

32

73 a

a-Zearalanol

49 (98)

1

+

47 c

ß-Zearalanol

45 (90)

5

+

50 c

Zearalenone

30 (60)

20

65 b

'+' Significant differentiation on the basis of %2(p < test

Mean values marked with the same letter in the last column do not differ significantly according to Duncan's multiple range test (p < 0.05)

aIn brackets percent of headed plants in population

Table 15.4 The influence of the inhibitor of zearalenone (malathion) on the generative development of winter wheat plants. Seeds of wheat cv. 'Grana' were cultured at sterile condition on Murashige and Skoog (1962) media supplemented with 0 (control), melathion (10 ml/dm3) and zearalenone (2 mg/dm3) during 5 weeks at 5°C (optimal time of vernalization). After vernalization plants were replaced to soil and grown at 20/17°C. Percentage of headed plants and the length of phase from vernalization to flowering was determined for 100 plants in each kind of medium

Table 15.4 The influence of the inhibitor of zearalenone (malathion) on the generative development of winter wheat plants. Seeds of wheat cv. 'Grana' were cultured at sterile condition on Murashige and Skoog (1962) media supplemented with 0 (control), melathion (10 ml/dm3) and zearalenone (2 mg/dm3) during 5 weeks at 5°C (optimal time of vernalization). After vernalization plants were replaced to soil and grown at 20/17°C. Percentage of headed plants and the length of phase from vernalization to flowering was determined for 100 plants in each kind of medium

Length of phase from vernalization

Medium

Percent of headed plants

to flowering (days)

Malathion

16

74

Zearalenon

100

57

0 (Control)

72

77

Biochemical analysis indicated that the stimulation of the generative differentiation in wheat shoot apices after short vernalization, but in the presence of zearalenone was connected with an intensified emission of heat and a decrease in the value of the electric potential of the cells (Biesaga-Koscielniak 2001). Additionally, during vernalization of these plants and after vernalization, zearalenone induced changes in the composition of fatty acids in the fractions of membrane glycolipids and phospholipids. Zearalenone treatment resulted in the increase in content unsaturated fatty acids (calculated as 18:3 to 18:2 ratio). Such an increase in fatty acid unsaturation is usually a result of changes in cell membranes being exposed to low temperatures. On the other hand, zearalenone somewhat hampered the adjustment of the fluidity of the cell membranes, which was indicated by an increase in the content of campesterol and cholesterol in the seedlings. The observed dual effect of this substance on membrane composition is that it can stabilize membrane structure at low temperature, which allows specific domains located on membranes to become more prominent.

Such changes may be involved in the pathway of induction of generative development of winter plants induced by vernalization. The involvement of zearalenone in the vernalization process was suggested by Meng et al. (1996) who indicated two specific zearalenone-binding proteins (39.8 and 12.5 kDa) in the vernalized embryos of winter wheat. They postulated that these proteins might act as activators of certain genes controlling the vernalization process in plants.

The role of zearalenone in generative induction was also confirmed in photoperiodic plants (Meng et al. 1992, 1996; Fu et al. 1995, 2000), which suggests its importance in flowering stimulation. In the short-day plant L. perpusilla 6746 and the long-day plant L. gibba G3, zearalenone enhanced flowering. In the day-neutral tobacco (Nicotiana tabacum L. cv. Samsun), zearalenone was one of the important flower stimuli and was related to the flower gradient in shoots (Meng et al. 1996). In the studies of Fu et al. (2000) a connection between zearalenone and flower bud formation in thin-cell layer explants of N. tabacum L was indicated. During the formation of flower buds, the authors observed two peaks in the endogenous zearalenone level, one at day 3 and the other at day 9 after the outset of the culture. The inhibitor of zearalenone biosynthesis (malathion), inhibited the biosynthesis of endogenous zearalenone and at the same time flower bud neoformation. Exogenous zearalenone application reduced the effect of malathion and stimulated flower bud neoformation.

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