β-Glucuronidase activity in seedlings of the parasitic angiosperm Cusctua pentagona: developmental impact of the β-glucuronidase inhibitor saccharic acid 1,4-lactone
Mark A. Schoenbeck A B , Gabriel A. Swanson A and Sydney J. Brommer AA Biology Department, University of Nebraska at Omaha, Omaha, NE 68182-0040, USA.
B Corresponding author. Email: mschoenbeck@mail.unomaha.edu
Functional Plant Biology 34(9) 811-821 https://doi.org/10.1071/FP07134
Submitted: 28 May 2007 Accepted: 18 July 2007 Published: 30 August 2007
Abstract
Endogenous plant β-glucuronidase (β-GUS) activity was detected in germinating seeds, seedlings, stems, flowers and haustoria of the parasitic angiosperm Cuscuta pentagona Engelm. In vitro characterisation of this activity showed it to have an acidic pH optimum, similar to previously characterised plant activities, and a sensitivity to the β-GUS inhibitor saccharic acid 1,4-lactone (SAL). Application of SAL to seeds immediately after chemical scarification resulted in a significant developmental delay and, frequently, in the total arrest of seedling growth. In contrast, application of SAL subsequent to the emergence of the radicle did not produce a significant effect on the development of the seedling. Thus, the distribution of activity and the developmentally contingent potency of SAL in inhibiting growth suggest a role for β-GUS at an early stage of seed germination or seedling growth. Further, the inability of the inhibitor to prevent subsequent shoot elongation suggests that at least some plant growth processes do not require this activity, or that it is required only at minimal levels and is unaffected by the application of SAL.
Additional keywords: germination, glycosyl hydrolase, seedling development.
Acknowledgements
The authors would like to thank Dr Carol Baskin and Gehan Jayasuria of the University of Kentucky for their kind assistance in interpreting histochemical staining patterns in Cuscuta seeds. We also thank Dr Claudia Rauter for performing the statistical analysis of seed germination and seedling growth data.
Albert M,
Werner M,
Proksch P,
Fry SC, Kaldenhoff R
(2004) The cell wall-modifying xyloglucan endotransglycosylase/hydrolase LeXTH1 is expressed during the defense reaction of tomato against the plant parasite Cuscuta reflexa. Plant Biology 6, 402–407.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Alwen A,
Moreno RM,
Vicente O, Heberle-Bors E
(1992) Plant endogenous β-glucuronidase activity: how to avoid interference with the use of the E. coli β-glucuronidase as a reporter gene in transgenic plants. Transgenic Research 1, 63–70.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bayer EM,
Bottrill AR,
Walshaw J,
Vigouroux M,
Naldrett MJ,
Thomas CL, Maule AJ
(2006) Arabidopsis cell wall proteome defined using multidimensional protein identification technology. Proteomics 6, 301–311.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bonfig KB,
Berger S,
Fatima T,
González MC, Roitsch T
(2007) Metabolic control of seedling development by invertases. Functional Plant Biology 34, 508–516.
| Crossref | GoogleScholarGoogle Scholar |
Deeks SJ,
Shamoun SF, Punja ZK
(1999) Tissue culture of parasitic flowering plants: methods and applications in agriculture and forestry. In Vitro Cellular & Developmental Biology. Plant 35, 369–381.
| Crossref | GoogleScholarGoogle Scholar |
Fry SC
(2004) Primary cell wall metabolism: tracking the careers of wall polymers in living plant cells. The New Phytologist 161, 641–675.
| Crossref | GoogleScholarGoogle Scholar |
Furuhashi K,
Kanno M, Morita T
(1995) Photocontrol of parasitism in a parasitic flowering plant, Cuscuta japonica Chois, cultured in vitro. Plant & Cell Physiology 36, 533–536.
Haidar MA,
Orr GL, Westra P
(1997) Effects of light and mechanical stimulation on coiling and prehaustorial formation in Cuscuta spp. Weed Research 37, 219–228.
| Crossref | GoogleScholarGoogle Scholar |
Haupt S,
Oparka KJ,
Sauer N, Neumann S
(2001) Macromolecular trafficking between Nicotiana tabacum and the holoparasite Cuscuta reflexa. Journal of Experimental Botany 52, 173–177.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hodal L,
Bochardt A,
Nielsen JE,
Mattsson O, Okkels F
(1992) Detection, expression, and specific elimination of endogenous β-glucuronidase activity in transgenic and non-transgenic plants. Plant Science 87, 115–122.
| Crossref | GoogleScholarGoogle Scholar |
Hutchison JM, Ashton FM
(1979) Effect of desiccation and scarification on the permeability and structure of the seed coat of Cuscuta campestris. American Journal of Botany 66, 40–46.
| Crossref | GoogleScholarGoogle Scholar |
Jefferson RA,
Burgess SM, Hirsch D
(1986) β-Glucuronidase from Escherichia coli as a gene fusion marker. Proceedings of the National Academy of Sciences of the United States of America 83, 8447–8451.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Jefferson RA,
Kavanagh TA, Bevan MW
(1987) GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in plants. The EMBO Journal 6, 3901–3907.
| PubMed |
Jeschke WD,
Bäumel P,
Räth N,
Czygan FC, Proksch P
(1994) Modelling of the flows and partitioning of carbon and nitrogen in the holoparasite Cuscuta reflexa Roxb. and its host Lupinus albus L.: II. Flows between host and parasite and within the parasitized host. Journal of Experimental Botany 45, 801–812.
| Crossref | GoogleScholarGoogle Scholar |
Karunairatnam MC, Levvy GA
(1949) The inhibition of β-glucuronidase by saccharic acid and the role of the enzyme in glucuronide synthesis. The Biochemical Journal 44, 599–604.
| PubMed |
Lee KB, Lee CD
(1989) The structure and development of the haustorium in Cuscuta australis. Canadian Journal of Botany 67, 2975–2982.
Levvy GA
(1954) Baicalinase, a plant β-glucuronidase. The Biochemical Journal 58, 462–469.
| PubMed |
Lyshede OB
(1984) Seed structure and germination in Cuscuta pedicellata with some notes on C. campestris. Nordic Journal of Botany 4, 669–674.
Lyshede OB
(1989) Electron microscopy of the filiform seedling axis of Cuscuta pedicellata. Botanical Gazette (Chicago, Ill.) 150, 230–238.
| Crossref | GoogleScholarGoogle Scholar |
Lyshede OB
(1992) Studies on mature seeds of Cuscuta pedicellata and C. campestris by electron microscopy. Annals of Botany 69, 365–371.
Maheshwari R,
Shailini C,
Veluthambi K, Mahadevan S
(1980) Interaction of gibberellic acid and indole-3-acetic acid in the growth of excised Cuscuta shoot tips in vitro. Plant Physiology 65, 186–192.
| PubMed |
Morimoto S,
Tateishi N,
Matsuda T,
Tanaka H,
Taura F,
Furuya N,
Matsuyama N, Shoyama Y
(1998) Novel hydrogen peroxide metabolism in suspension cells of Scutellaria baicalensis Georgi. Journal of Biological Chemistry 273, 12606–12611.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Nagar R,
Singh M, Sanwal GG
(1984) Cell wall degrading enzymes in Cuscuta reflexa and its hosts. Journal of Experimental Botany 35, 1104–1112.
| Crossref | GoogleScholarGoogle Scholar |
Neyland R
(2001) A phylogeny inferred from large ribosomal subunit (26S) rDNA sequences suggests that Cuscuta is a derived member of Convolvulaceae. Brittonia 53, 108–115.
Plegt L, Bino RJ
(1989) β-Glucuronidase activity during development of the male gametophyte from transgenic and non-transgenic plants. Molecular & General Genetics 216, 321–327.
| Crossref | GoogleScholarGoogle Scholar |
Rao PN, Rama Rao PV
(1990) Not embryos but seedlings in seeds of Cuscuta. Indian Journal of Botany 13, 159–160.
Roney JK,
Khatibi PA, Westwood JH
(2007) Cross-species translocation of mRNA from host plants into the parasitic plant dodder. Plant Physiology 143, 1037–1043.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Runyon JB,
Mescher MC, DeMoraes MC
(2006) Volatile chemical cues guide host location and host selection by parasitic plants. Science 313, 1964–1967.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sasaki K,
Taura F,
Shoyama Y, Morimoto S
(2000) Molecular characterization of a novel β-glucuronidase from Scutellaria baicalensis Georgi. Journal of Biological Chemistry 275, 27466–27472.
| PubMed |
Schulz M, Weissenbock G
(1987) Partial purification of a luteolin-triglucuronide-specific β-glucuronidase from rye primary leaves (Secale cereale). Phytochemistry 26, 933–937.
| Crossref | GoogleScholarGoogle Scholar |
Shi HZ,
Yang HY, Zhou C
(1995) Intrinsic GUS activity in various tissues and during pollen development of Nicotiana tabacum. Acta Botanica Sinica 37, 134–139.
Stephanovic S, Olmstead RG
(2004) Testing the phylogenetic position of a parasitic plant (Cuscuta, Convolvulaceae, Asteridae): Bayesian inference and the parametric bootstrap on data drawn from three genomes. Systematic Biology 53, 384–399.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sudan C,
Prakash S,
Bhomkar P,
Jain S, Bhalla-Sarin N
(2006) Ubiquitous presence of β-glucuronidase (GUS) in plants and its regulation in some model plants. Planta 224, 853–864.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Vaughn KC
(2002) Attachment of the parasitic weed dodder to the host. Protoplasma 219, 227–237.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Vaughn KC
(2003) Dodder hyphae invade the host: a structural and immunocytochemical characterization. Protoplasma 220, 189–200.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Vaughn KC
(2006) Conversion of the searching hyphae of dodder into xylic and phloic hyphae: a cytochemical and immunocytochemical investigation. International Journal of Plant Sciences 167, 1099–1114.
| Crossref | GoogleScholarGoogle Scholar |
Wen F,
Woo HH,
Hirsch AM, Hawes MC
(2004) Lethality of inducible, meristem-localized ectopic β-glucuronidase expression in plants. Plant Molecular Biology Reporter 22, 7–14.
Woo HH,
Jeong BR,
Hirsch AM, Hawes MC
(2007) Characterization of Arabidopsis AtUGT85A and AtGUS gene families and their expression in rapidly dividing tissues. Genomics 90, 143–153.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
