Effects of endophyte transmission on ecophysiological characteristics of Achnatherum sibiricum

doi:10.17521/cjpe.2015.0008

Abstract

Abstract: Aims

Achnatherum sibiricum plants were infected by fungal endophytes Neotyphodium and Epichloëand high infection rates have been found in our experimental field. Our objective was to determine the effects of Neotyphodium and Epichloë on growth and physiological characteristics in A. sibiricum.

Methods

In a field experiment, we measured plant growth and physiological characteristics of A. sibiricum with a LI-6400 portable photosynthesis system and determined the contents of carbon (C%) and nitrogen (N%) and other physiological variables in 2011 and 2012. Achnatherum sibiricum plants were successfully infected with Neotyphodium and Epichloë.

Important findings

Neotyphodium infection had a significant positive effect on both leaf length and plant height in A. sibiricum, whereas Epichloë infection had a significant negative effect on the two variables. Maximum net photosynthetic rate was significantly higher in the endophyte-free plants than in plants infected by Neotyphodium and Epichloë; whilst Neotyphodium infected plants had significantly higher maximum net photosynthetic rate than Epichloë infected plants. Moreover, Neotyphodium infection significantly increased stomatal limitation and water use efficiency (WUE) of the host grass. Epichloë infection had a negative effect on photosynthetic variables except intercellular CO₂ concentration in the first year. Neotyphodium infection resulted in greater accumulation of soluble sugars in host plants than Epichloë infection and endophyte-free treatment. The N% in Epichloë infected plant was significantly higher than in Neotyphodium infected plants in both years and in endophyte-free plants in the second year.

Key words: Neotyphodium, Epichloë, Achnatherum sibiricum

JIA Tong,REN An-Zhi,WEI Mao-Ying,YIN Li-Jia,GAO Yu-Bao. Effects of endophyte transmission on ecophysiological characteristics of Achnatherum sibiricum[J]. Chin J Plan Ecolo, 2015, 39(1): 72-80.

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URL: https://www.plant-ecology.com/EN/10.17521/cjpe.2015.0008

https://www.plant-ecology.com/EN/Y2015/V39/I1/72

Figures/Tables 8

Fig. 1 Effects of Epichloë and Neotyphodium infection on growth of Achnatherum sibiricum in 2011 (mean ± SE). Different lowercase letters indicate signiﬁcant differences at the 0.05 level. EF, endophyte-free plant; Ep, plant infected by Epichloë; Ne, plant infected by Neotyphodium.

Fig. 2 Effects of Epichloë and Neotyphodium infection on growth of Achnatherum sibiricum in 2012 (mean ± SD). Different lowercase letters indicate signiﬁcant differences at the 0.05 level. EF, endophyte-free plant; Ep, plant infected by Epichloë; Ne, plant infected by Neotyphodium.

Fig. 3 Effects of Epichloë and Neotyphodium infection on specific leaf area in Achnatherum sibiricum (mean ± SD). Different lowercase letters indicate signiﬁcant differences at the 0.05 level. EF, endophyte-free plant; Ep, plant infected by Epichloë; Ne, plant infected by Neotyphodium.

Fig. 4 The influence of Epichloë and Neotyphodium infection on photosynthetic pigments in Achnatherum sibiricum in 2011 (mean ± SE). Different lowercase letters indicate signiﬁcant differences at the 0.05 level. EF, endophyte-free plant; Ep, plant infected by Epichloë; Ne, plant infected by Neotyphodium. Car, carotene; Chl a, chlorophyll a; Chl b, chlorophyll b.

Fig. 5 The influence of Epichloë and Neotyphodium infection on maximum net photosynthetic rate in Achnatherum sibiricum (mean ± SE). Different lowercase letters indicate signiﬁcant differences at the 0.05 level. EF, endophyte-free plant; Ep, plant infected by Epichloë; Ne, plant infected by Neotyphodium.

Table 1 The comparison of fitted values of photosynthetic characteristics in Achnatherum sibiricum

Year		蒸腾速率 Transpiration rate (mmol·m^-2·s^-1)	气孔导度 Stomatal conductance (mol·m^-2·s^-1)	胞间CO₂浓度 Intercellular CO₂ concentration (μmol·mol^-1)	气孔限制值 Stomatal limitation	水分利用效率 Water use efﬁciency (mmol·mmol^-1)	光能利用效率 Light use efﬁciency (μmol·μmol^-1₎
2011	Ep	5.83^b	0.33^b	320.6^a	0.19^c	2.035^c	0.009 8^c
	Ne	4.76^c	0.30^b	294.8^c	0.26^a	3.086^a	0.012 1^b
	EF	6.47^a	0.42^a	306.1^b	0.23^b	2.712^b	0.014 5^a
2012	Ep	2.07^c	0.09^c	210.47^b	0.48^b	4.52^a	0.008^c
	Ne	2.44^b	0.09^b	199.80^b	0.51^a	4.53^a	0.009^b
	EF	3.45^a	0.15^a	249.13^a	0.38^c	3.74^b	0.011^a

Fig. 6 Effects of Epichloë and Neotyphodium infection on soluble sugar and total phenolic contents in 2011 and the total nonstructural carbohydrate in 2012 in Achnatherum sibiricum (mean ± SD). A, Soluble sugar content. B, Total phenolic content. C, Total nonstructural carbohydrate content. Different lowercase letters indicate signiﬁcant differences at the 0.05 level. EF, endophyte-free plant; Ep, plant infected by Epichloë; Ne, plant infected by Neotyphodium.

Fig. 7 Effects of Epichloë and Neotyphodium infection on nitrogen content, carbon content and C:N in Achnatherum sibiricum in 2012 (mean ± SD). Different lowercase letters indicate signiﬁcant differences at the 0.05 level. EF, endophyte-free plant; Ep, plant infected by Epichloë; Ne, plant infected by Neotyphodium.

References 33

1	Bradshaw AD, Snaydon RW (1959). Population differentiation within plant species in response to soil factors. Nature, 183, 129-130.
2	Bucheli E, Leuchtmann A (1996). Evidence for genetic
3	differentiation between choke-inducing and asymptomtic strains of the Epichloë grass endophyte from Brachy- podium sylvaticum.Evolution, 50, 1879-1887.
4	Bultman TL, Leuchtmann A (2003). A test of host specialization by insect vectors as a mechanism for reproductive isolation among entomophilous fungal species. Oikos, 103, 681-687.
5	Cheplick GP, Cho R (2003). Interactive effects of fungal endophyte infection and host genotype on growth and storage in Lolium perenne. New Phytologist, 158, 183-191.
6	Cheplick GP, Chui T (2001). Effects of competitive stress on vegetative growth, storage, and regrowth after defoliation in Phleum pratense. Oikos, 95, 291-299.
7	Cheplick GP, Faeth S (2009). Ecology and Evolution of the Grass-endophyte Symbiosis. Oxford University Press, Oxford, UK.
8	Clay K (1990). Fungal endophytes of grasses. Annual Review of Ecology and Systematics, 21, 275-297.
9	da Silveira AJ, Feitosa TFF, Stull JW (1978). A rapid technique for total nonstructural carbohydrate determination of plant tissue. Journal of Agricutural and Food Chemistry, 26, 770-772.
10	de Battista JP, Bacon CW, Severson R, Plattner RD, Bouton JH (1990). Indole acetic acid production by the fungal endophyte of tall fescue. Agronomy Journal, 82, 878-880.
11	Donaghy DJ, Fulkerson WJ (1997). The importance of water-soluble carbohydrate reserves on regrowth and root growth of Lolium perenne (L.). Grass and Forage Science, 52, 401-407.
12	Donaghy DJ, Fulkerson WJ (1998). Priority for allocation of water-soluble carbohydrate reserves during regrowth of Lolium perenne. Grass and Forage Science, 53, 211-218.
13	Elmi AA, West CP (1995). Endophyte infection effects on stomatal conductance, osmotic adjustment and drought recovery of tall fescue. New Phytologist, 131, 61-67.
14	Groppe K, Steinger T, Sanders I, Schmid B, Wiemken A, Boller T (1999). Interaction between the endophytic fungus Epichloe bromicola and the grass Bromus erectus: Effects of endophyte infection, fungal concentration and environment on grass growth and flowering. Molecular Ecology, 8, 1827-1835.
15	Hunt MG, Rasmussen S, Newton PCD, Parsons AJ, Newman JA (2005). Near-term impacts of elevated CO2, nitrogen and fungal endophyte-infection on Lolium perenne L. growth, chemical composition and alkaloid production. Plant, Cell & Environment, 28, 1345-1354.
16	Ji YL, Wang ZW, Yu HS, Wang SM (2003). Neotyphodium uncinatum, an endophytic fungus obtained from Festuca arundinacea Schreb. Journal of Nanjing Agricultural University, 26(2), 47-50.
	(in Chinese with English abstract) [纪燕玲, 王志伟, 于汉寿, 王世梅 (2003). 分离自苇状羊茅(Festucaa rundinacea Schreb.)的内生真菌Neotyphodium uncinatum. 南京农业大学学报, 26(2), 47-50.]
17	Kover PX, Clay K (1998). Trade-off between virulence and vertical transmission and the maintenance of a virulent plant pathogen. The American Naturalist, 152, 165-175.
18	Leuchtmann A, Schardl CL, Siegel MR (1994). Sexual compatibility and taxonomy of a new species of Epichloe symbiotic with fine Fescue grasses. Mycologia, 86, 802-812.
19	Leuchtmann A, Schmidt D, Bush LP (2000). Different levels of protective alkaloids in grasses with stroma-forming and seed-transmitted Epichloë/Neotyphodium endophytes. Jou- rnal of Chemical Ecology, 26, 1025-1036.
20	Li X, Han R, Ren AZ, Gao YB (2010). Using high-temperature treatment to construct endophyte-free Achnatherum sibiricum. Microbiology China, 37, 1395-1400.
	[李夏, 韩荣, 任安芝, 高玉葆 (2010). 高温处理构建不感染内生真菌羽茅种群的方法探讨. 微生物学通报, 37, 1395-1400.]
21	Malinowski DP, Alloush GA, Belesky DP (1998). Evidence for chemical changes on the root surface of tall fescue in response to infection with the fungal endophyte Neotyphodium coenophialum. Plant and Soil, 205, 1-12.
22	Malinowski DP, Belesky DP (2000). Adaptations of endophyte-infected cool-season grasses to environmental stresses: Mechanisms of drought and mineral stress tolerance. Crop Science, 40, 923-940.
23	Marks S, Clay K, Cheplick GP (1991). Effects of fungal endophytes on interspecific and intraspecific competition in the grasses Festuca arundinacea and Lolium perenne. Journal of Applied Ecology, 28, 194-204.
24	Moon CD, Craven KD, Leuchtmann A, Clement SL, Schardl CL (2004). Prevalence of interspecific hybrids amongst asexual fungal endophytes of grasses. Molecular Ecology, 13, 1455-1467.
25	Morse LJ, Day TA, Faeth SH (2002). Effect of Neotyphodium endophyte infection on growth and leaf gas exchange of Arizona fescue under contrasting water availability regimes. Environmental and Experimental Botany, 48, 257-268.
26	Rasmussen S, Parsons AJ, Bassett S, Christensen MJ, Hume DE, Johnson LJ, Johnson RD, Simpson WR, Stacke C, Voisey CR, Xue H, Newman JA (2007). High nitrogen supply and carbohydrate content reduce fungal endophyte and alkaloid concentration in Lolium perenne. New Phytologist, 173, 787-797.
27	Sánchez FJ, Manzanares M, de Andres EF, Tenorio JL, Ayerbe L (1998). Turgor maintenance, osmotic adjustment and soluble sugar and proline accumulation in 49 pea cultivars in response to water stress. Field Crops Research, 59, 225-235.
28	Schardl CL, Leuchtmann A, Spiering MJ (2004). Symbioses of grasses with seedborne fungal endophytes. Annual Review of Plant Biology, 55, 315-340.
29	Shen J, Tao WW, Chen C, Chen YG, Wang ZW (2009). Review on the grass endophyte research in China 9―Seed transmission characteristics and distribution in host plants of Epichloё yangzii. Pratacultural Science, 26, 146-151.
	(in Chinese with English abstract) [申靖, 陶文文, 陈昌, 陈永敢, 王志伟 (2009). 禾本科植物内生真菌研究9——Epichloё yangzii的种传特性及其在宿主体内的分布. 草业科学, 26, 146-151.]
30	Tintjer T, Leuchtmann A, Clay K (2008). Variation in horizontal and vertical transmission of the endophyte Epichloë elymi infecting the grass Elymus hystrix. New Phytologist, 179, 236-246.
31	Wei YK, Gao YB, Zhang X, Su D, Wang YH, Xu H, Lin F, Ren AZ, Chen L, Nie LY (2007). Distribution and diversity of Epichloë/Neotyphodium fungal endophytes from different populations of Achnatherum sibiricum (Poaceae) in the Inner Mongolia Steppe, China. Fungal Diversity, 24, 329-345.
32	White JF (1988). Endophyte-host associations in forage grasses. XI. A proposal concerning origin and evolution. Mycologia, 80, 442-446.
33	Zhang YP, Nan ZB (2007). Distribution of Epichloë endophytes in Chinese populations of Elymus dahuricus and variation in peramine levels. Symbiosis, 43, 13-19.