#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Sugar, amino acid and inorganic ion profiling of the honeydew from different hemipteran species feeding on Abies alba and Picea abies


Autoři: Basel Shaaban aff001;  Victoria Seeburger aff002;  Annette Schroeder aff002;  Gertrud Lohaus aff001
Působiště autorů: Molecular Plant Science / Plant Biochemistry, University of Wuppertal, Wuppertal, Germany aff001;  Apicultural State Institute, University of Hohenheim, Stuttgart, Germany aff002
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0228171

Souhrn

Several hemipteran species feed on the phloem sap of plants and produce large amounts of honeydew that is collected by bees to produce honeydew honey. Therefore, it is important to know whether it is predominantly the hemipteran species or the host plant to influence the honeydew composition. This is particularly relevant for those botanical and zoological species from which the majority of honeydew honey originates. To investigate this issue, honeydew from two Cinara species located on Abies alba as well as from two Cinara and two Physokermes species located on Picea abies were collected. Phloem exudates of the host plants were also analyzed. Honeydew of all species contained different proportions of hexoses, sucrose, melezitose, erlose, and further di- and trisaccharides, whereas the phloem exudates of the host trees contained no trisaccharides. Moreover, the proportions of sugars differed significantly between hemipteran species feeding on the same tree species. Sucrose hydrolysis and oligosaccharide formation was shown in whole-body homogenates of aphids. The type of the produced oligosaccharides in the aphid-extracts correlated with the oligosaccharide composition in the honeydew of the different aphid species. The total contents of amino acids and inorganic ions in the honeydew were much lower than the sugar content. Glutamine and glutamate were predominant amino acids in the honeydew of all six hemipteran species and also in the phloem exudates of both tree species. Potassium was the dominant inorganic ion in all honeydew samples and also in the phloem exudate. Statistical analyses reveal that the sugar composition of honeydew is determined more by the hemipteran species than by the host plant. Consequently, it can be assumed that the sugar composition of honeydew honey is also more influenced by the hemipteran species than by the host tree.

Klíčová slova:

Amino acid analysis – Aphids – Fructoses – Honey – Insects – Phloem – Plants – Sucrose


Zdroje

1. Douglas AE. Phloem-sap feeding by animals: problems and solutions. J Exp Bot. 2006; 57: 747–754. doi: 10.1093/jxb/erj067 16449374

2. Fink D, Dobbelstein E, Barbian A, Lohaus G. Ratio of sugar concentrations in the phloem sap and the cytosol of mesophyll cells in different tree species as an indicator of the phloem loading mechanism. Planta. 2018; 248: 661–673. doi: 10.1007/s00425-018-2933-7 29882156

3. Lohaus G, Moellers C. Phloem transport of amino acids in two Brassica napus L. genotypes and one B. carinata genotype in relation to their seed protein content. Planta. 2000; 211: 833–840. doi: 10.1007/s004250000349 11144268

4. Woodring J, Wiedemann R, Fischer M K, Hoffmann K H, Völkl W. Honeydew amino acids in relation to sugars and their role in the establishment of ant-attendance hierarchy in eight species of aphids feeding on tansy (Tanacetum vulgare). Physiol Entomol. 2004; 29: 311–319.

5. Nadwodnik J, Lohaus G. Subcellular concentrations of sugar alcohols and sugars in relation to phloem translocation in Plantago major, Plantago maritima, Prunus persica, and Apium graveolens. Planta. 2008; 227: 1079–1089. doi: 10.1007/s00425-007-0682-0 18188589

6. Öner-Sieben S, Lohaus G. Apoplastic and symplastic phloem loading in Quercus robur and Fraxinus excelsior. J Exp Bot. 2014; 65: 1905–1916. doi: 10.1093/jxb/eru066 24591056

7. Karley AJ, Douglas AE, Parker WE. Amino acid composition and nutritional quality of potato leaf phloem sap for aphids. J Exp Biol. 2002; 205: 3009–3018. 12200404

8. Lohaus G, Schwerdtfeger M. Comparison of sugars, iridoid glycosides and amino acids in nectar and phloem sap of Maurandya barclayana, Lophospermum erubescens, and Brassica napus. PLoS ONE. 2014; 9(1): e87689. doi: 10.1371/journal.pone.0087689 24489951

9. Sandström JP, Moran NA. Amino acid budgets in three aphid species using the same host plant. Physiol Entomol. 2001; 26: 202–211.

10. Wilkinson TL, Ashford DA, Pritchard J, Douglas AE. Honeydew sugars and osmoregulation in the pea aphid Acyrthosiphon pisum. J Exp Biol 1997; 200: 2137–2143. 9320049

11. Febvay G, Rahbé Y, Rynkiewicz M, Guillaud J, Bonnot G. Fate of dietary sucrose and neosynthesis of amino acids in the pea aphid, Acyrthosiphon pisum, reared on different diets. J Exp Biol. 1999; 202: 2639–2652. 10482723

12. Auclair J. Aphid feeding and nutrition. Ann Rev Entomol. 1963; 8: 439–490.

13. Leroy P, Wathelet B, Sabri A, Francis F, Verheggen F, Capella Q, et al. Aphid-host plant interactions: does aphid honeydew exactly reflect the host plant amino acid composition? Arthropod-Plant Interact. 2011; 5: 193–199.

14. Sabri A, Vandermoten S, Leroy PD, Haubruge E, Hance T, Thonart P, et al. Proteomic investigation of aphid honeydew reveals an unexpected diversity of proteins. PloS ONE. 2013; 8: e74656. doi: 10.1371/journal.pone.0074656 24086359

15. Völkl W, Woodring J, Fischer M, Lorenz MW, Hoffmann KH. Ant-aphid mutualisms: the impact of honeydew production and honeydew sugar composition on ant preferences. Oecologia. 1999; 118: 483–491. doi: 10.1007/s004420050751 28307416

16. Fischer MK, Völkl W, Schopf R, Hoffmann KH. Age-specific pattern in honeydew production and honeydew composition in the aphid Metopeurum fuscoviride: implications for ant-attendance. J Insect Physiol. 2002; 48: 319–326. doi: 10.1016/s0022-1910(01)00179-2 12770106

17. Hendrix DL, Wei Y, Legget JE. Homopteran honeydew is determined by both the insect and the plant species. Comp Biochem Physiol. 1992; 101: 23–27.

18. Fischer MK, Shingleton AW. Host plant and ants influence the honeydew sugar composition of aphids. Funct Ecol. 2001; 15: 544–550.

19. Bacon JSD, Dickinson B. The origin of melezitose: a biochemical relationship between the lime tree (Tilia spp.) and an aphis (Eucallipterus tiliae L.). Biochem. 1957; 66: 289–297.

20. Liebig G. Gaschromatographische und enzymatische Untersuchungen des Zuckerspektrums des Honigtaus von Buchneria pectinatae (Nördl.) Apidologie. 1979; 10: 213–225.

21. Mittler TE. Studies on the feeding and nutrition of Tuberolachnus salignus (Gmelin) (Homoptera, Aphididae). II. The nitrogen and sugar composition of ingested phloem sap and excreted honeydew. J Exp Biol. 1958; 35: 74–84.

22. Fisher DB, Wright JP, Mittler TE. Osmoregulation by the aphid Myzus persicae: a physiological role for honeydew oligosaccharides. J Insect Physiol. 1984; 30: 387–393.

23. Rhodes JD, Croghan PC, Dixon AFG. Dietary sucrose and oligosaccharide synthesis in relation to osmoregulation in the pea aphid, Acythosiphon pisum. Physiol Entomol. 1997; 22: 373–379.

24. Ashford DA, Smith WA, Douglas AE. Living on a high sugar diet: the fate of sucrose ingested by a phloem feeding insect, the pea aphid Acyrthosiphon pisum. J Insect Physiol. 2000; 46: 335–341. doi: 10.1016/s0022-1910(99)00186-9 12770238

25. Walters FS, Mullin CA. Sucrose-dependent increase in the oligosaccharide production and associated glycosidase activities in the potato aphid Macrosiphum euphorbiae (Thomas). Arch Insect Biochem Physiol. 1988; 9: 35–46.

26. Braendle C, Miura T, Bickel R, Shingleton AW, Kamphampati S, Stern DL. Developmental origin and evolution of bacteriocytes in the aphid-Buchnera symbiosis. PLoS Biol. 2003; 1: e1. doi: 10.1371/journal.pbio.0000001

27. Prosser WA, Douglas AE. A test of the hypothesis that nitrogen is upgraded and recycled in an aphid (Acythosiphon pisum) symbiosis. J Insect Physiol. 1992; 38: 93–99.

28. Sasaki T, Ishikawa H. Production of essential amino acids from glutamate by mycetocyle symbionts of the pea aphid, Acythosiphon pisum maintained on artificial diets. J Insect Physiol. 1995; 37: 749–756.

29. Wilkinson TL, Adams D, Minto LB, Douglas AE. The impact of host plant on the abundance and function of symbiotic bacteria in an aphid. J Exp Biol. 2001; 204: 3027–3028. 11551991

30. Kunkel H, Kloft, Die Honigtau-Erzeuger des Waldes W. J., in: Kloft W.J. and Kunkel H. (Eds.), Waldtracht und Waldhonig in der Imkerei. Ehrenwirth, Munich. 1985; pp. 48–265.

31. Ruoff K, Luginbühl W, Kilchenmann V, Bosset JO., von der Ohe K, von der Ohe W, et al. Authentication of the botanical origin of honey using profiles of classical measurands and discriminant analysis. Apidologie. 2007; 38: 438–452.

32. Nottbohm FE, Lucius F. Melezitose im Honigtauhonig der Linde. Zeitschrift für Untersuchungen der Lebensmittel. 1929; 57: 549–558.

33. Hudson CS, Sherwood SF. The occurrence of melezitose in honey. J Am Chem Soc. 1920; 42: 116–125.

34. Gölz H. Der Melezitosegehalt im Honigtau verschiedener Lachnidenarten. Apidologie. 1982; 13: 89–91.

35. Zoebelein G. Die Rolle des Waldhonigtaus im Nahrungshaushalt forstlich nützlicher Insekten. Forstw Centralbl. 1957; 76: 24–34.

36. Hijaz F, Killiny N. Collection and chemical composition of phloem sap from Citrus sinensis L. Osbeck (Sweet Orange). PLoS ONE. 2014 9(7): e101830. doi: 10.1371/journal.pone.0101830 25014027

37. Findling S, Zanger K, Krueger S, Lohaus G. Subcellular distribution of raffinose oligosaccharides and other metabolites in summer and winter leaves of Ajuga reptans (Lamiaceae). Planta. 2015; 241: 229–241. doi: 10.1007/s00425-014-2183-2 25269399

38. Göttlinger T, Schwerdtfeger M, Tiedge K, Lohaus G. What do nectarivorous bats like? Nectar composition in Bromeliaceae with special emphasis on bat-pollinated species. Front Plant Sci. 2019; 10: 205. doi: 10.3389/fpls.2019.00205 30847001

39. West SG, Finch JF, Curran PJ. Structural equation models with nonnormal variables: problems and remedies. In: Hoyle RH, editor. Structural equation modeling: Concepts, issues and applications. Newbery Park, CA: Sage; 1995. p56–75.

40. Hervé MR, Nicolè F, Lê Cao KA. Multivariate analysis of multiple datasets: a practical guide for chemical ecology. J Chem Ecol. 2018; 44: 215–234. doi: 10.1007/s10886-018-0932-6 29479643

41. Ramette A. Multivariate analyses in microbial ecology. FEMS Microbiol Ecol. 2007; 62: 142–160. doi: 10.1111/j.1574-6941.2007.00375.x 17892477

42. Oksanen J, Kindt R, Legendre P, O’Hara B, Henry M, Stevens H. The vegan package. Community ecology package. R package version 2.5–3 [online]. 2007; https://CRAN.R-project.org/package=vegan (accessed on 07 October 2019).

43. Anderson MJ. A new method for non-parametric multivariate analysis of variance. Austral Ecology. 2001; 26: 32–46.

44. Anderson MJ. Distance-based tests for homogeneity of multivariate dispersions. Biometrics. 2006; 62: 245–253. doi: 10.1111/j.1541-0420.2005.00440.x 16542252

45. Anderson MJ, Walsh DCI. PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: what null hypothesis are you testing? Ecol Monogr. 2013; 83: 557 574.

46. Ziegler H, Mittler TE. Über den Zuckergehalt der Siebröhren- bzw- Siebzellensäfte von Heracleum mantegazzianum und Picea abies (L.) Karst Z Naturforschung. 1959; 14 B: 278–281.

47. Cristofoletti PT, Ribeiro AF, Deraison C, Rahbe Y, Terra WR. Midgut adaption and digestive enzyme distribution in a phloem feeding insect, the pea aphid Acyrthosiphon pisum. J Insect Physiol 2003; 49: 11–24. doi: 10.1016/s0022-1910(02)00222-6 12770012

48. Weibull J, Ronquist F, Brishammar, S. Free amino acid composition of leaf exudates and phloem sap. Plant Physiol. 1990; 92: 222–226. doi: 10.1104/pp.92.1.222 16667250

49. Haribal M, Jander G. Stable isotope studies reveal pathways for the incorporation of non-essential amino acids in Acyrthosiphon pisum (pea aphids). J Exp Biol. 2015; 218: 3797–3806. doi: 10.1242/jeb.129189 26632455

50. Sasaki T, Fukuchi N, Ishikawa H. Amino acid flow through aphid and its symbiont: studies with 15N-labeled glutamine. Zool Sci. 1993; 10: 787–791.

51. Ehrhardt P. Die anorganischen Bestandteile des Honigtaues von Megoura viciae Buckt. Experientia. 1965; XXI/8: 472–473.

52. Downing N. The regulation of sodium, potassium and chloride in an aphid subjected to ionic stress. J Exp Biol. 1980; 87: 343–349.

53. Wyatt GR. The biochemistry of insect haemolymph. Ann Review Entomol. 1961; 6: 75–102.

54. Fermo P, Beretta G, Facino RM, Gelmini F. Ionic profile of honey as a potential indicator of botanical origin and global environmental pollution. Environ Pollution. 2013; 178: 173–181.

55. Tiedge K, Lohaus G. Nectar sugars and amino acids in day- and night-flowering Nicotiana species are more strongly shaped by pollinators’ preferences than organic acids and inorganic ions. PLoS ONE. 2017; 12(5): e0176865. doi: 10.1371/journal.pone.0176865 28467507

56. Schmelz H, Gall H, Fehlinger GF, Heider E, Rösch J. Alle Jahre wieder Ratlosigkeit–oder was tun bei Melezitosetracht. ADIZ. 2002; 1: 23–24

57. Imdorf A, Bogdanov S, Kilchenmann V. Zementhonig im Honig- und Brutraum–was dann? Schweizer Zentrum für Bienenforschung. 2002; 1: 1–16.


Článek vyšel v časopise

PLOS One


2020 Číslo 1
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

KOST
Koncepce osteologické péče pro gynekology a praktické lékaře
nový kurz
Autoři: MUDr. František Šenk

Sekvenční léčba schizofrenie
Autoři: MUDr. Jana Hořínková

Hypertenze a hypercholesterolémie – synergický efekt léčby
Autoři: prof. MUDr. Hana Rosolová, DrSc.

Svět praktické medicíny 5/2023 (znalostní test z časopisu)

Imunopatologie? … a co my s tím???
Autoři: doc. MUDr. Helena Lahoda Brodská, Ph.D.

Všechny kurzy
Kurzy Podcasty Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#