Journal of Plant Growth Regulation

, Volume 38, Issue 1, pp 249–261 | Cite as

Temperature and Hormones Associated with Bacterial Etiolation Symptoms of Creeping Bentgrass and Annual Bluegrass

  • Sha Liu
  • Joseph Vargas
  • Emily MerewitzEmail author


Bacterial etiolation, caused by Acidovorax avenae or Xanthomonas translucens pv. poae, is a problematic disease of creeping bentgrass (Agrostis stolonifera) and annual bluegrass (Poa annua) turfgrass stands. The objective of this study was to determine whether temperature may play a role in phytohormone production by these bacteria and to determine if there is any change in phytohormones specifically in etiolated plant tissues. In vitro, A. avenae and X. translucens were cultured at 25, 30, 35 and 40 °C for 14 days. Bacterial cultures were sampled for gibberellic acid isoforms (GA1, GA3, GA4, and GA20), jasmonic acid, salicylic acid (SA), indole-3-acetic acid (IAA), zeatin riboside, and abscisic acid (ABA). No phytohormones were detected in pure cultures of X. translucens, whereas A. avenae produced GA1, GA3, GA4, and IAA. Acidovorax avenae isolate MSU-13 produced significantly higher GA1 and GA3 at 35 and 40 °C on most days measured. In the field study, etiolated stem and leaf tissues of creeping bentgrass and annual bluegrass were evaluated for bacterial identification, etiolation ratings, and phytohormone quantification. Significantly more etiolation symptoms were observed in both annual bluegrass and creeping bentgrass on days with higher temperatures. In annual bluegrass, etiolated stems and leaves showed significantly higher GA1, GA3, etiolated leaves showed significantly higher GA20, ABA, and lower IAA compared to normal turf tissues on most experimental dates. In creeping bentgrass, higher GA1, GA4, SA, ABA, and lower IAA were detected in etiolated turf tissues than normal tissues on most experimental dates. Plant hormone regulation due to the presence of bacteria may be altered differentially in response to different bacteria species eliciting similar plant symptoms.


Agrostis stolonifera Poa annua Acidovorax avenae Xanthomonas translucens pv. poae Bacteria etiolation Temperature Phytohormone 



The authors wish to thank the Michigan Turfgrass Foundation and AgBioResearch of Michigan State University for funding of this project.

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflicts of interest.


  1. Alcázar R, Parker JE (2011) The impact of temperature on balancing immune responsiveness and growth in Arabidopsis. Trends Plant Sci 16:666–675. CrossRefGoogle Scholar
  2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410.CrossRefGoogle Scholar
  3. Atkinson NJ, Urwin PE (2012) The interaction of plant biotic and abiotic stresses: from genes to the field. J Exp Bot 63(10):3523–3543CrossRefGoogle Scholar
  4. Bottini R, Cassán F, Piccoli P (2004) Gibberellin production by bacteria and its involvement in plant growth promotion and yield increase. Appl Microbiol Biotechnol 65:497CrossRefGoogle Scholar
  5. Fett WF, Osman SF, Dunn MF (1987) Auxin production by plant-pathogenic pseudomonads and xanthomonads. Appl Environ Microbiol 53(8):1839–1845Google Scholar
  6. Finegold MS, Martin WJ (1982) Diagnostic microbiology chapt. 3. Mosby Co., St. LouisGoogle Scholar
  7. Giordano PR (2014) Identification and characterization of a new bacterial disease of creeping bentgrass (Agrostis stolonifera L.) caused by Acidovorax avenae subsp. avenae. Ph.D. Thesis. Michigan State University, Michigan, USA, pp. 89Google Scholar
  8. Giordano PR, Vargas JM, Detweiler AR, Dykema NM, Yan L (2010) First report of a bacterial disease on creeping bentgrass (Agrostis stolonifera) caused by Acidovorax spp. in the United States. Plant Dis 94(7):922CrossRefGoogle Scholar
  9. Giordano PR, Chaves AM, Mitkowski NA, Vargas JM (2012) Identification, characterization, and distribution of Acidovorax avenae subsp. avenae associated with creeping bentgrass etiolation and decline. Plant Dis 96:1736–1742CrossRefGoogle Scholar
  10. Hayashi S, Gresshoff PM, Ferguson BJ (2014) Mechanistic action of gibberellins in legume nodulation: gibberellin and nodulation. J Integr Plant Biol 56:971–978. CrossRefGoogle Scholar
  11. Huot B, Castroverde CDM, Velásquez AC et al (2017) Dual impact of elevated temperature on plant defence and bacterial virulence in Arabidopsis. Nat Commun 8:1808. CrossRefGoogle Scholar
  12. Karadeniz A, Topcuoğlu ŞF, İnan S (2006) Auxin, gibberellin, cytokinin and abscisic acid production in some bacteria. World J Microbiol Biotechnol 22:1061. CrossRefGoogle Scholar
  13. Krishnan SK, Merewitz E (2015) Drought stress and trinexapac-ethyl modify phytohormone content within kentucky bluegrass leaves. J Plant Growth Regul 34:1–12. CrossRefGoogle Scholar
  14. Krishnan SK, Ma Y, Merewitz E (2016) Leaf trimming and high temperature regulation of phytohormones and polyamines in creeping bentgrass leaves. J Am Soc Hortic Sci 141:66–75CrossRefGoogle Scholar
  15. Latin R, Hopkins DL (1995) Bacterial fruit blotch of watermelon. Plant Dis 79:761–765CrossRefGoogle Scholar
  16. Liu S (2016) Phytohormones associated with bacterial disease of creeping bentgrass(Agrostis stolonifera) caused by Acidovorax avenae subsp. avenae. Master Thesis. Michigan State University, Michigan, USA, pp. 63–88Google Scholar
  17. Liu J, Zhao Z, Teffera Y (2012) Application of on-line nano-liquid chromatogra-phy/mass spectrometry in metabolite identification studies. Rapid Commun Mass Spectrom 26:320–326CrossRefGoogle Scholar
  18. Liu S, Vargas J, Merewitz E (2017) Phytohormones associated with bacterial etiolation disease in creeping bentgrass. Environ Exp Bot 133:35–49CrossRefGoogle Scholar
  19. Mazzella N, Molinet J, Syakti AD, Dodi A, Doumenq P, Artaud J, Bertrand JC (2004) Bacterial phospholipid molecular species analysis by ion-pair reversed-phase HPLC/ESI/MS. J Lipid Res 45:1355–1363. CrossRefGoogle Scholar
  20. Mitkowski NA, Browning M, Basu C, Jordan K, Jackson N (2005) Pathogenicity of Xanthomonas translucens from annual bluegrass on golf course putting greens. Plant Dis 89:469–473CrossRefGoogle Scholar
  21. Olszewski N, Sun T, Gubler F (2002) Gibberellin signaling: biosynthesis, catabolism, and response pathways. Plant Cell 14:S61–S80CrossRefGoogle Scholar
  22. Roberts D, Vargas J, Detweiler R (1985) Occurrence of bacterial wilt on Poa annua and other turfgrasses. (Abstract). Phytopathology 75:1289Google Scholar
  23. Roberts JA, Tredway LP, Ritchie DF (2014) First report of Xanthomonas translucens causing etiolation on creeping bentgrass turf in illinois, kentucky, and north Carolina. Plant Dis 98:839CrossRefGoogle Scholar
  24. Roberts JA, Ritchie DF, Kerns JP (2015) Bacterial etiolation of creeping bentgrass as influenced by biostimulants and trinexapac-ethyl. Crop Prot 72:119–126CrossRefGoogle Scholar
  25. Roberts JA, Ritchie DF, Kerns JP (2016) Plant growth regulator effects on bacterial etiolation of creeping bentgrass putting green turf caused by Acidovorax avenae. Plant Dis 3:577–582CrossRefGoogle Scholar
  26. Roberts JA, Ma B, Tredway LP, Ritchie DF, Kerns JP (2018) Identification and pathogenicity of bacteria associated with etiolation and decline of creeping bentgrass golf course putting greens. Phytopathology 108:23–30CrossRefGoogle Scholar
  27. Ross JJ, Willis CL, Gaskin P, Reid J, Planta (1992) Shoot elongation in Lathyrus odoratus L.: gibberellin levels in light- and dark-grown tall and dwarf seedlings. Planta 187:10. CrossRefGoogle Scholar
  28. Sands DC, Schroth MN, Hildebrand DC (1980) Pseudomonas. In: Schaad NW (ed) Laboratory guide for identification of plant pathogenic bacteria. American Phytopathological Society, St. Paul, pp 36–44Google Scholar
  29. Sauter M, Kende H (1992) Gibberellin-induced growth and regulation of the cell division cycle in deepwater rice. Planta 188(3):362–368. CrossRefGoogle Scholar
  30. Scarcella ASA, Bizarria R Jr, Bastos RG, Magri MMR (2017) Temperature, pH and carbon source affect drastically indole acetic acid production of plant growth promoting yeasts. Braz J Chem Eng 34(2):429–438CrossRefGoogle Scholar
  31. Schaad NW (2008) Emerging plant pathogenic bacteria and global warming. In: Fatmi MB, Collmer A, Iacobellis NS, Masfield JW, Murillo J, Schaad NW, Ulrich M (eds) Pseudomonas syringae pathovars and related pathogens: identification epidemiology and genomics. Springer, Dordrecht, pp 369–372CrossRefGoogle Scholar
  32. Spray CR, Kobayashi M, Suzuki Y, Phinney BO, Gaskin P, MacMillan J (1996) The dwarf-1 (d1) mutant of Zea mays blocks three steps in the gibberellin-biosynthetic pathway. Proc Natl Acad Sci USA 93:10515–10518CrossRefGoogle Scholar
  33. Sun T (2010) Gibberellin signal transduction in stem elongation & leaf growth. In: Davies PJ (ed) Plant hormones. Springer, DordrechtGoogle Scholar
  34. Takahashi N, Phinney BO, MacMillan J (eds) (1991) Gibberellins. Springer-Verlag, New YorkGoogle Scholar
  35. Talon M, Zeevaart JA (1992) Stem elongation and changes in the levels of gibberellins in shoot tips induced by differential photoperiodic treatments in the long-day plant Silene armeria. Planta 188(4):457–461. CrossRefGoogle Scholar
  36. Thorn G, Tsuneda A (1996) Molecular genetic characterization of bacterial isolates causing brown blotch on cultivated mushrooms in Japan. Mycoscience 37:409–416CrossRefGoogle Scholar
  37. Uozu S, Tanaka-Ueguchi M, Kitano H, Hattori K, matsuoka M (2000) Characterization of XET-related genes of rice. Plant Physiol 122:853–859CrossRefGoogle Scholar
  38. Van den Heuvel KJPT, Barendse GWM, Wullem GJ (2001) Effect of gibberellic acid on cell division and cell elongation in anthers of the gibberellin deficient gib-1 mutant of tomato. Plant Biol 3(2):124–131CrossRefGoogle Scholar
  39. Wilkinson KG, Dixon KW, Sivasithamparam K, Ghisalberti EL (1994) Effect of IAA on symbiotic germination of an Australian orchid and its production by orchid-associated bacteria. Plant Soil 159:291–295CrossRefGoogle Scholar
  40. Zeng Q, Wang J, Bertels F, Giordano PR, Chilvers MI, Huntley RB, Vargas JM, Sundin GW, Jacobs JL, Yang CH (2017) Recombination of virulence genes in divergent Acidovorax avenae strains that infect a common host. Mol Plant Microbe Interact 30:813–828CrossRefGoogle Scholar
  41. Zhou T, Neal JC (1995) Annual bluegrass (Poa annua) control with Xanthomonas campestris pv. poannua in New York state. Weed Technol 9:173–177CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Plant, Soil, and Microbial SciencesMichigan State UniversityMichiganUSA

Personalised recommendations