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IPBRG Investigators: Spence Behmer, Wei Chen

 

Collaborators: Angela Douglas (Cornell University), Bob Grebenok (Canisius College),
                        Heiko Vogel (Max Planck Institute for Chemical Ecology),
                        Keyan Zhu-Salzman (Texas A&M University)

Sterols serve three critical functions in insects: (1) they are important components of cellular membranes, (2) they are precursors for many hormones (e.g. 20-OH ecdysone) and (3) they play a role in regulating genes involved in developmental processes. Insects, however, differ from most other animals in that they have a dietary requirement for sterols because they lack the ability to biosynthesise sterols. Cholesterol (right) is the dominant sterol found in most insects, but since plants rarely contain it, insect herbivores must either metabolise plant sterols or use them as they are. Cholesterol is characterized by a double bond at position 5, and no alkyl group on the side chain.

 

At least 100 different sterols have been identified in plants (e.g. sitosterol, stigmasterol and spinasterol - see below), but metabolic constraints in insects can limit the range of phytosterols that can be converted to cholesterol. We are interested in how small structural differences can influence insect behaviour and physiology, including utilisation and metabolism, and the manner in which these subtle differences can influence evolutionary processes.

 

Variation in Plant Sterol Structure. Sitosterol is the most abundant and common plant sterol. It has a double bond at position 5 (similar to cholesterol), but like most plant sterols it has an alkyl group (green structure) on the side chain. Stigmasterol is another relatively common plant sterol. In contrast to sitosterol, it has a double bond at position 22 on the side chain. Spinasterol, a plant sterol found in spinach, also has a double bond at position 22, but differs from sitosterol and stigmasterol by having a double bond at position 7 in the sterol nucleus. From a grasshoppers point of view, sitosterol is a "good" sterol since it can be metabolised to cholesterol. On the other hand, stigmasterol and spinasterol are considered "bad" sterols since they cannot be metabolised to cholesterol (for more details, see Behmer et al. 1999b).

Our early research into insect sterol biology was conducted on grasshoppers, and in these insects we find that extreme sterol metabolic constraints are a shared trait (Behmer and Elias 2000). Particularly fascinating, though, is that grasshoppers suffer high levels of mortality when they accumulate unmetabolized "bad" sterols above a certain threshold, even if the proper amount of a "good" sterol is obtained (Behmer and Elias 1999a, 2000). It remains unknown, however, whether this is due to interruption of cell structural features or an inability to make the important cholesterol-derived steroid hormones.

 

More recently we have been looking at sterol use in a range of pest caterpillars and hemipterans, both on artificial diets with different sterol combinations, and on transgenically modified tobacco and Arabidopsis plants. The early caterpillar work was part of Xiangfeng Jing's Ph.D. research, and was funded by a grant from the USDA (w/ Bob Grebenok). We also received funding from the USDA to examine sterol use in aphids (in collaboration with Angela Douglas and Bob Grebenok); this grant also examined sterol profiles in hemipterans more broadly. We are currently on our third round of USDA funding. Our most recent project is a collaborative effort (Bob Grebenok, Keyan Zhu-Salzman and Heiko Vogel) where we are manipulating plant sterol profiles using RNAi techniques, and investigating molecular aspects of insect sterol use (in caterpillars).

Relevant Publications:

 

Jing, X., Grebenok, R.J. and Behmer, S.T. (2014) Balance matters: How the ratio of dietary

     steroids affects caterpillar development, growth and reproduction. Journal of Insect
     Physiology
 67: 85-96. [pdf]

 

Bouvaine, S., Faure, M-L., Grebenok, R. J., Behmer, S.T., and Douglas, A.E. (2014)

     A dietary test of putative deleterious sterols for the aphid Myzus persicae.

     PLoS ONE 9, e86256. [pdf]

 

Jing, X., Grebenok, R.J., Behmer, S.T. (2013) Sterol/steroid metabolism and absorption in a
     generalist and specialist caterpillar: Effects of dietary sterol/steroid structure, mixture
     and ratio.
Insect Biochemistry and Molecular Biology 43, 580-587. [pdf]

 

Thompson, B.M., Grebenok, R.J., Behmer, S.T., and Gruner, D.S. (2013) Microbial
     symbionts shape the sterol profile of the xylem-feeding woodwasp, Sirex noctilio.
     Journal of Chemical Ecology 39, 129-139.
[pdf]

 

Behmer, S.T., Olszewski, N., Sebastiani, J., Palka, S., Sparacino, G., Sciarrno, E., and
     Grebenok, R.J. (2013) Plant phloem sterol content: forms, putative functions,
     and implications for phloem-feeding insects. Frontiers in Plant
     Science
4, 370. [pdf]

 

Jing, X., Grebenok, R.J., and Behmer, S.T. (2012) Plant sterols and host plant suitability for
     generalist and specialist caterpillars.
Journal of Insect Physiology 58, 235-244.
     [pdf]

 

Bouvaine, S., Behmer, S.T., Lin, G.G., Faure, M-L., Grebenok, R.J., and Douglas, A.E. (2012)
     The physiology of sterol nutrition in the pea aphid Acyrthosiphon pisum. Journal of
     Insect Physiology
. [pdf]

 

Behmer, S.T., Grebenok, R.J., and Douglas, A.E. (2011) Plant sterols and host plant suitability
     for a phloem-feeding insect. Functional Ecology 25, 484-491. [pdf]

 

Janson, E.M. Grebenok, R.J., Behmer, S.T., and Abbot, P. (2009) Same host-plant, different
     sterols: variation in sterol metabolism in an insect herbivore community. Journal of
     Chemical Ecology
. 35, 1309-1319. [pdf]

 

Behmer, S.T. and Nes, W. D. (2003) Insect sterol nutrition and physiology: a global
     overview.
Advances in Insect Physiology 31, 1-72. [pdf]

 

Behmer, S.T. and Elias, D.O. (2000) Sterol metabolic constraints as a factor contributing
     to the maintenance of
diet mixing in grasshoppers (Orthoptera: Acrididae). Physiological
     and Biochemical Zoology
73, 219-230.
[pdf]

 

Behmer, S.T., Elias, D.O. and Bernays, E.A. (1999a) Post-ingestive feedbacks and
     associative learning regulate
the intake of unsuitable sterols in a generalist
     grasshopper. The Journal of Experimental Biology 202, 739-748
. [pdf]

 

Behmer, S.T., Elias, D.O. and Grebenok, R.J. (1999b) Phytosterol metabolism and
     absorption in the generalist
grasshopper Schistocerca americana (Orthoptera: Acrididae).
     Archives of Insect Biochemistry and Physiology 42, 13-25.
[pdf]

 

Behmer, S.T. and Elias, D.O. (1999a) The nutritional significance of sterol metabolic
     constraints in the
generalist grasshopper Schistocerca americana. Journal of Insect
     Physiology
45, 339-348.
[pdf]

 

Behmer, S.T. and Elias, D.O. (1999b) Phytosterol structure as a basis of food aversion
     learning in the
grasshopper Schistocerca americana (Orthoptera: Acrididae).
     Physiological Entomology 24, 18-27.
[pdf]

 

Behmer, S.T. and Grebenok, R.J. (1998) Impact of dietary sterols on life-history traits of
     a caterpillar.
Physiological Entomology 23, 165-175.

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