Skip to main content

Water-Deficit Stress Tolerance Differs between Two Locoweed Genera (Astragalus and Oxytropis) with Fungal Endophytes

  • Nina Klypina (a1), Matthew Pinch (a1), Brian J. Schutte (a1), Janakiraman Maruthavanan (a1) and Tracy M. Sterling (a2)...

Locoweeds are plants of the genera Astragalus and Oxytropis (Fabaceae family) and are toxic to cattle, sheep, and horses. The toxic property of locoweeds is due to the alkaloid swainsonine (SWA), which is synthesized by an endophytic fungus Alternaria spp. section Undifilum. Although the endophyte–locoweed complex is often considered mutualistic, empirical evidence for benefits to host plants is lacking. This study: 1) compared the growth, photosynthesis, and leaf pigment and antioxidant concentrations between endophyte-infected and endophyte-free plants under well-watered and water-deficit conditions; and 2) measured SWA to determine whether SWA concentrations are attenuated by water deficit and leaf age. Locoweed species in this study were woolly loco and silky crazyweed. Endophyte-infected and endophyte-free (by removal of seed coat) seedlings, as confirmed by DNA analyses, were grown under greenhouse conditions for 6 mo, after which plants were subjected to three 12- to 15-d water-deficit periods that created sublethal drought conditions. Results suggest that the endophyte did not influence photosynthetic gas exchange and leaf pigment concentrations. Under well-watered conditions only, endophyte-infected woolly loco plants had lower shoot and root biomass and higher concentrations of α-tocopherol than endophyte-free plants. SWA analyses revealed taxon-specific effects of water deficit, with water deficit increasing SWA concentrations in young leaves of woolly loco but not affecting SWA concentration in silky crazyweed. These results suggest that the endophyte behaves as a parasite in woolly loco plants grown under optimal but not under water-limited conditions. Further, results indicate that drought conditions elevate the toxicity of woolly loco plants. Improved understanding of endophyte-locoweed interactions and factors influencing SWA levels will contribute to the development of livestock management strategies to predict toxicity in particular locoweed populations.

Corresponding author
*Corresponding author’s E-mail:
Hide All

Associate Editor for this paper: Vijay Nandula, USDA–ARS

Hide All
Baucom, DL, Romero, M, Belfon, R, Creamer, R (2012) Two new species of Undifilum, fungal endophytes of Astragalus (locoweeds) in the United States. Botany 90:866875
Braun, K, Romero, J, Liddell, C, Creamer, R (2003) Production of swainsonine by fungal endophytes of locoweed. Mycol Res 107:980988
Casas, C, Torretta, JP, Exeler, N, Omacini, M (2016) What happens next? Legacy effects induced by grazing and grass-endophyte symbiosis on thistle plants and their floral visitors. Plant Soil 405:211229
Chenna, R, Sugawara, H, Koike, T, Lopez, R, Gibson, TJ, Higgins, DG, Thompson, JD (2003) Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res 31:34973500
Clay, K (1993) The ecology and evolution of endophytes. Agric Ecosyst Environ 44:39
Clay, K, Schardl, CL (2002) Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Amer Nat 160:S99S127
Cook, D, Gardner, DR, Grum, DS, Pfister, JA, Ralphs, MH, Welch, KD, Green, BT (2011) Swainsonine and endophyte relationships in Astragalus mollissimus and Astragalus lentiginosus . J Agric Food Chem 59:12811287
Cook, D, Gardner, DR, Ralphs, MH, Pfister, JA, Welch, KD, Green, BT (2009) Swainsonine concentrations and endophyte amounts of Undifilum oxytropis in different plant parts of Oxytropis sericea . J Chem Ecol 35:12721278
Cook, D, Grum, DS, Gardner, D, Welch, KD, Pfister, JA (2013) Influence of endophyte genotype on swainsonine concentrations in Oxytropis sericea . Toxicon 61:105111
Cook, D, Shi, L, Gardner, DR, Pfister, JA, Grum, D, Welch, KD, Ralphs, MH (2012) Influence of phenological stage on swainsonine and endophyte concentrations in Oxytropis sericea . J Chem Ecol 38:195203
Creamer, R, Baucom, D (2013) Fungal endophytes of locoweeds: a commensal relationship? J Plant Physiol Pathol 1:25
Delaney, KJ, Klypina, N, Maruthavanan, J, Lange, C, Sterling, TM (2011) Locoweed dose responses to nitrogen: positive for biomass and primary physiology, but inconsistent for an alkaloid. Amer J Bot 98:19561965
Dreyer, DL, Jones, KC, Molyneux, RJ (1985) Feeding deterrency of some pyrrolizidine, indolizidine, and quinolizidine alkaloids towards pea aphid (Acyrthosiphon pisum) and evidence for phloem transport of indolizidine alkaloid swainsonine. J Chem Ecol 11:10451051
Elbein, AD, Solf, R, Dorling, PR, Vosbeck, K (1981) Swainsonine: an inhibitor of glycoprotein processing. Proc Natl Acad Sci USA 78:73937397
Faeth, SH (2009) Asexual fungal symbionts alter reproductive allocation and herbivory over time in their native perennial grass hosts. Amer Nat 173:554565
Faeth, SH, Sullivan, TJ (2003) Mutualistic asexual endophytes in a native grass usually parasitic. Amer Nat 161:310325
Fox, WE, Allred, KW, Roalson, EH (1998) A Guide to Common Locoweeds and Milkvetches of New Mexico. Las Cruces, NM: New Mexico State University Agriculture Experiment Station and Cooperative Extension Service Cir 557. 95 p. Accessed December 1, 2016
Gardner, DR, Molyneux, RJ, Ralphs, MH (2001) Analysis of swainsonine: extraction methods, detection, and measurement in populations of locoweeds (Oxytropis spp.). J Agric Food Chem 49:45734580
Guo, L, Qiu, J, Han, Z, Ye, Z, Chen, C, Liu, C, Xin, X, Ye, C, Wang, Y, Xie, H, Wang, Yu, Bao, J, Tang, S, Xu, J, Gui, Y, Fu, F, Wang, W, Zhang, X, Zhu, Q, Guang, X, Wang, C, Cui, H, Cai, D, Ge, S, Tuskan, GA, Yang, X, Qian, Q, He, SY, Wang, J, Zhou, X, Fan, L (2015) A host plant genome (Zizania latifolia) after a century‐long endophyte infection. Plant Journal 83:600609
Hamilton, CE, Gundel, PE, Helander, M, Saikkonen, K (2012) Endophytic mediation of reactive oxygen species and antioxidant activity in plants: a review. Fungal Div 54:110
James, LF, Hartley, WJ, Van Kampen, KM (1981) Syndromes of Astragalus poisoning in livestock. J Amer Vet Assoc 178:146150
James, LF, Nielsen, DB, Panter, KE (1992) Impact of poisonous plants on the livestock industry. J. Range Manage 45:38
Kannadan, S, Rudgers, JA (2008) Endophyte symbiosis benefits a rare grass under low water availability. Function Ecol 22:706713
Kulshreshtha, S, Creamer, R, Sterling, TM (2004) Phylogenetic relationships among New Mexico Astragalus mollissimus varieties and Oxytropis species by restriction fragment analysis. Weed Sci 52:984988
Lawrence, DP, Rotondo, F, Gannibal, PB (2016) Biodiversity and taxonomy of the pleomorphic genus Alternaria . Mycol Prog 15:122
Li, YZ, Nan, YB (2007) A new species, Embellisia astragali sp. nov., causing standing milk-vetch disease in China. Mycologia 99:406411
Malinkowsky, DP, Belesky, DP (2000) Adaptations of endophyte-infected cool-season grasses to environmental stresses: mechanisms of drought and mineral stress tolerance. Crop Sci 40:923940
McLain-Romero, J, Creamer, R, Zepeda, H, Strickland, J, Bell, G (2004) The toxicosis of Embellisia fungi from locoweed (Oxytropis lambertii) is similar to locoweed toxicosis in rats. J Anim Sci 82:21692174
Oldrup, E, McLain-Romero, J, Padilla, A, Moya, A, Gardner, D, Creamer, R (2010) Localization of endophytic Undifilum fungi in locoweed seed and influence of environmental parameters on a locoweed in vitro culture system. Botany 88:512521
Pfister, JA, Stegelmeier, BL, Gardner, DR, James, LF (2003) Grazing of spotted locoweed (Astragalus lentiginosus) by cattle and horses in Arizona. J Anim Sci 81:22852293
Pryor, BM, Creamer, R, Shoemaker, RA, McLain-Romero, J, Hambleton, S (2009) Undifilum, a new genus for endophytic Embellisia oxytropis and parasitic Helminthosporium bornmuelleri on legumes. Botany 87:178194
Ralphs, MH, Cook, D, Gardner, DR, Grum, DS (2011) Transmission of the locoweed endophyte to the next generation of plants. Fungal Ecol 4:251255
Ralphs, MH, Creamer, R, Baucom, D, Gardner, DR, Welsh, SL, Graham, JD, Hart, C, Cook, D, Stegelmeier, BL (2008) Relationship between the endophyte Embellisia spp. and the toxic alkaloid swainsonine in major locoweed species (Astragalus and Oxytropis). J Chem Ecol 34:3238
Ralphs, MH, Panter, KE, James, LF (1990) Feed preferences and habituation of sheep poisoned by locoweed. J Anim Sci 68:13541362
Ralphs, MH, Welsh, SL, Gardner, DR (2002) Distribution of the locoweed toxin swainsonine in populations of Oxytropis lambertii . J Chem Ecol 28:701707
Ratnayaka, HH, Molin, WT, Sterling, TM (2003) Physiological and antioxidant responses of cotton and spurred anoda under interference and mild drought. J Exper Bot 54:22932305
Ravel, C, Courty, C, Coudret, A, Charmet, G (1997) Beneficial effects of Neotyphodium lolii on the growth and the water status in perennial ryegrass cultivated under nitrogen deficiency or drought stress. Agronomie 17:173181
Rodriguez, R, Redman, R (2005) Balancing the generation and elimination of reactive oxygen species. Proc Natl Acad Sci USA 102:31753176
Rodriguez, RJ, Henson, J, Van Volkenburgh, E, Hoy, M, Wright, L, Beckwith, F, Kim, YO, Redman, RS (2008) Stress tolerance in plants via habitat-adapted symbiosis. ISME J 2:404416
Rodriguez, RJ, White, JF Jr, Arnold, AE, Redman, RS (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314330
Saikkonen, K, Faeth, SH, Helander, M, Sullivan, TJ (1998) Fungal endophytes: a continuum of interactions with host plants. Annu Rev Ecol System 29:319343
Saikkonen, K, Lehtonen, P, Helander, M, Koricheva, J, Faeth, SH (2006) Model systems in ecology: dissecting the endophyte-grass literature. Trends Plant Sci 11:428433
Schutte, BJ, Klypina, N, Ashigh, J (2014) Endophyte effects on locoweed (Astragalus mollissimus) growth responses to increasing temperature and intraspecific competition. Page 45 in Proceedings of the 67th Western Society of Weed Science, Colorado Springs, CO: Western Society of Weed Science
Singh, LP, Gill, SS, Tutega, N (2011) Unraveling the role of fungal symbionts in plant abiotic stress tolerance. Plant Signal Behav 6:175191
Stegelmeier, BL, James, LF, Panter, KE, Ralphs, MH, Gardner, DR, Molyneux, RJ, Pfister, JA (1999) The pathogenesis and toxicokinetics of locoweed (Astragalus and Oxytropis spp.) poisoning in livestock. J Natural Toxins 8:3545
Thompson, DC, Knight, JL, Sterling, TM, Murray, LW (1995) Preference for specific varieties of woolly locoweed by a specialist weevil, Cleonidius trivittatus. Southwest Entomol 20:325333
Thompson, JD, Higgins, DG, Gibson, TJ (2004) Clustal-W-improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res 22:46734680
Torell, LA, Owen, LP, McDaniel, KC, Graham, D (2000) Perceptions and economic losses from locoweed in north-eastern New Mexico. J Range Manage 53:376383
Vallotton, AD, Murray, LW, Delaney, KJ, Sterling, TM (2012) Water deficit induces swainsonine of some locoweed taxa, but with no swainsonine-growth trade-off. Acta Oecologia 43:140149
Wang, Q, Nagao, H, Li, YL, Wang, HS, Kakishima, M (2006) Embellisia oxytropis, a new species isolated from Oxytropis kansuensis in China. Mycotaxon 95:255260
White, JF Jr, Torres, MS (2010) Is plant endophyte-mediated defensive mutualism the result of oxidative stress protection? Physiol Plant 138:440446
Woudenberg, JHC, Groenewald, JZ, Binder, M, Crous, PW (2013) Alternaria redefined. Stud Mycol 75:171212
Zhao, BY, Liu, ZY, Wang, JJ, Sun, LS, Wang, ZX, Wang, YC (2009) Isolation and NMR study on swainsonine from locoweed, Astragalus strictus . Agr Sci China 8:115120
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Weed Science
  • ISSN: 0043-1745
  • EISSN: 1550-2759
  • URL: /core/journals/weed-science
Please enter your name
Please enter a valid email address
Who would you like to send this to? *



Full text views

Total number of HTML views: 3
Total number of PDF views: 37 *
Loading metrics...

Abstract views

Total abstract views: 193 *
Loading metrics...

* Views captured on Cambridge Core between 30th June 2017 - 25th May 2018. This data will be updated every 24 hours.