The influence of the hemiparasitic angiosperm Cassytha pubescens on photosynthesis of its host Cytisus scoparius
Hao Shen A B , Jane N. Prider B , José M. Facelli B and Jennifer R. Watling B CA South China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510650, China.
B School of Earth and Environmental Sciences, The University of Adelaide, Adelaide, SA 5005, Australia.
C Corresponding author. Email: jennifer.watling@adelaide.edu.au
Functional Plant Biology 37(1) 14-21 https://doi.org/10.1071/FP09135
Submitted: 4 June 2009 Accepted: 7 September 2009 Published: 5 January 2010
Abstract
Infection with Cassytha pubescens R.Br, an Australian native hemiparasitic plant, can lead to death of the invasive shrub, Cytisus scoparius L. Link (Scotch broom). We examined the influence of C. pubescens on photosynthetic physiology of C. scoparius to determine whether this might contribute to death of infected plants. Infected C. scoparius had significantly lower photosynthetic rates, stomatal conductance and transpiration, and higher Ci (internal [CO2]), than uninfected plants. Rapid light response curves, determined using chlorophyll fluorescence, indicated significantly lower light-saturated electron transport rates and lower quantum yields for infected plants relative to uninfected plants. However, Rubisco content did not differ between infected and uninfected plants, suggesting the lower photosynthetic rates were most likely due to stomatal closure, rather than lower photosynthetic capacity. As a consequence of lower assimilation rates, PSII efficiency was lower in infected plants than uninfected plants across the diurnal cycle. Infected plants also had significantly lower pre-dawn Fv/Fm values and slower recovery from exposure to high light than uninfected plants. Our results suggest that infected C. scoparius are more susceptible to photodamage than uninfected plants. Combined with lower carbon fixation rates, this could contribute to the poor performance and even death of infected plants.
Additional keywords: chlorophyll fluorescence, gas exchange, parasitic plant, photodamage, photoinhibition, Rubisco, water potential.
Acknowledgements
This work was supported by the Australian Research Council (grant number LP 0667863) and Linkage partners (Adelaide and Mount Lofty Ranges and South Australian Murray–Darling Basin Natural Resources Management Boards, SA Water, Forestry SA and SA Department of Water, Land and Biodiversity Conservation). Hao Shen was supported by a 6-month Chinese Academy of Sciences fellowship. We thank Professor Spencer Whitney (Australian National University) for his kind supply of the spinach Rubisco antibody and Nicole Grant for assistance with protein extraction.
Arnon DI
(1949) Copper enzymes in isolated chloroplasts: polyphenoloxidase in Beta vulgaris. Plant Physiology 24, 1–15.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bossard CC, Rejmanek M
(1992) Why have green stems? Functional Ecology 6, 197–205.
| Crossref | GoogleScholarGoogle Scholar |
Bradford MM
(1976) A rapid and sensitive method for the quantitation of microgram quantities of proteins utilizing the principle of protein-dye-binding. Analytical Biochemistry 72, 248–254.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Cameron DD,
Geniez JM,
Seel WE, Irving LJ
(2008) Suppression of host photosynthesis by the parasitic plant Rhinanthus minor. Annals of Botany 101, 573–578.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Cechin I, Press MC
(1993) Nitrogen relations of the sorghum–Striga hermonthica host–parasite association: growth and photosynthesis. Plant, Cell & Environment 16, 237–247.
| Crossref | GoogleScholarGoogle Scholar |
Clark J, Bonga JM
(1970) Photosynthesis and respiration in black spruce (Picea mariana) parasitized by eastern dwarf mistletoe (Arceuthobium pusillum). Canadian Journal of Botany 48, 2029–2031.
| Crossref | GoogleScholarGoogle Scholar |
Demmig-Adams B, Adams WW
(1992) Photoprotection and other responses of plants to light stress. Annual Review of Plant Physiology and Plant Molecular Biology 43, 599–626.
| Crossref | GoogleScholarGoogle Scholar |
Frost DL,
Gurney AL,
Press MC, Scholes JD
(1997) Striga hermonthica reduces photosynthesis in sorghum: the importance of stomatal limitations and a potential role for ABA? Plant, Cell & Environment 20, 483–492.
| Crossref | GoogleScholarGoogle Scholar |
Graves JD,
Press MC, Stewart GR
(1989) A carbon balance model of the sorghum–Striga hermonthica host–parasite association. Plant, Cell & Environment 12, 101–107.
| Crossref | GoogleScholarGoogle Scholar |
Gurney AL,
Press MC, Ransom JK
(1995) The parasitic angiosperm Striga hermonthica can reduce photosynthesis of its sorghum and maize hosts in the field. Journal of Experimental Botany 46, 1817–1823.
| Crossref | GoogleScholarGoogle Scholar |
Hibberd JM,
Quick WP,
Press MC, Scholes JD
(1996) The influence of the parasitic angiosperm Striga gesnerioides on the growth and photosynthesis of its host, Vigna unguiculata. Journal of Experimental Botany 47, 507–512.
| Crossref | GoogleScholarGoogle Scholar |
Hibberd JM,
Quick WP,
Press MC, Scholes JD
(1998) Can source–sink relations explain responses of tobacco to infection by the root holoparasitic angiosperm Orobanche cernua? Plant, Cell & Environment 21, 333–340.
| Crossref | GoogleScholarGoogle Scholar |
Jeschke WD, Hilpert A
(1997) Sink-stimulated photosynthesis and sink-dependent increase in nitrate uptake: nitrogen and carbon relations of the parasitic association Cuscuta reflexa–Ricinus communis. Plant, Cell & Environment 20, 47–56.
| Crossref | GoogleScholarGoogle Scholar |
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 |
Jeschke WD,
Bäumel P, Räth N
(1995) Partitioning of nutrients in the system Cuscuta reflexa–Lupinus albus. Aspects of Applied Biology 42, 71–79.
Jeschke WD,
Baig A, Hilpert A
(1997) Sink-stimulated photosynthesis, increased transpiration and increased demand-dependent stimulation of nitrate uptake: nitrogen and carbon relations in the parasitic association Cuscuta reflexa–Coleus blumei. Journal of Experimental Botany 48, 915–925.
| Crossref | GoogleScholarGoogle Scholar |
Laemmli UK
(1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.
| Crossref |
PubMed |
Maxwell K, Johnson GN
(2000) Chlorophyll fluorescence – a practical guide. Journal of Experimental Botany 51, 659–668.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
McLuckie J
(1924) Studies in parasitism. I. A contribution to the physiology of the genus Cassytha, Part 1. Proceedings of the Linnean Society of New South Wales 49, 55–78.
Prider J,
Watling J, Facelli JM
(2009) Impacts of a native parasitic plant on an introduced and a native host species: implications for the control of an invasive weed. Annals of Botany 103, 107–115.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ralph PJ, Gademann R
(2005) Rapid light curves: a powerful tool to assess photosynthetic activity. Aquatic Botany 82, 222–237.
| Crossref | GoogleScholarGoogle Scholar |
Ramlan MF, Graves JD
(1996) Estimation of the sensitivity to photoinhibition in Striga hermonthica-infected sorghum. Journal of Experimental Botany 47, 71–78.
| Crossref | GoogleScholarGoogle Scholar |
Shen H,
Hong L,
Ye WH,
Cao HL, Wang ZM
(2007) The influence of the holoparasitic plant Cuscuta campestris on the growth and photosynthesis of its host Mikania micrantha. Journal of Experimental Botany 58, 2929–2937.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Smith LH,
Keys AJ, Evans MCW
(1995) Striga hermonthica decreases photosynthesis in Zea mays through effects on leaf cell structure. Journal of Experimental Botany 46, 759–765.
| Crossref | GoogleScholarGoogle Scholar |
Taylor A,
Martin J, Seel WE
(1996) Physiology of the parasitic association between maize and witchweed (Striga hermonthica): is ABA involved? Journal of Experimental Botany 47, 1057–1065.
| Crossref | GoogleScholarGoogle Scholar |
Watling JR, Press MC
(1997) How is the relationship between the C4 cereal Sorghum bicolor and the C3 root hemi-parasites Striga hermonthica and Striga asiatica affected by elevated CO2? Plant, Cell & Environment 20, 1292–1300.
| Crossref | GoogleScholarGoogle Scholar |
Watling JR, Press MC
(2000) Infection with the parasitic angiosperm Striga hermonthica influences the response of the C3 cereal Oryza sativa to elevated CO2. Global Change Biology 6, 919–930.
| Crossref | GoogleScholarGoogle Scholar |
Watling JR, Press MC
(2001) Impacts of infection by parasitic angiosperms on host photosynthesis. Plant Biology 3, 244–250.
| Crossref | GoogleScholarGoogle Scholar |
White AJ, Critchley C
(1999) Rapid light curves: a new fluorescence method to assess the state of the photosynthetic apparatus. Photosynthesis Research 59, 63–72.
| Crossref | GoogleScholarGoogle Scholar |
Whitney SM, Andrews TJ
(2001) Plastome-encoded bacterial ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) supports photosynthesis and growth in tobacco. Proceedings of the National Academy of Sciences of the United States of America 98, 14738–14743.
| Crossref | GoogleScholarGoogle Scholar | PubMed |