Stocktake Sale on now: wide range of books at up to 70% off!
Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Photosynthesis, ionomics and metabolomics of the host–hemiparasite association Acacia gerrardiiViscum schimperi

Zouhaier Barhoumi https://orcid.org/0000-0002-1737-7571 A B *
+ Author Affiliations
- Author Affiliations

A Biology Department, King Khalid University, P.O. Box-9004, Abha 61413, Saudi Arabia.

B Laboratory of Extremophile Plants, Biotechnology Center of Borj Cedria, University Tunis El Manar, B.P. 901, Hammam-Lif, Tunis, Tunisia.

* Correspondence to: barhoumi_zou2000@yahoo.fr

Handling Editor: Thomas Roberts

Functional Plant Biology 51, FP23206 https://doi.org/10.1071/FP23206
Submitted: 26 May 2023  Accepted: 16 November 2023  Published: 1 December 2023

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Viscum schimperi is an evergreen hemiparasitic plant that can grow on stems and branches of several tree species. It penetrates the host tissues and forms a vascular bridge (haustorium) to withdraw the nutritive resources. Its relationships with hosts remain unknown. This study aimed to investigate the physiological and biochemical attributes of the host–hemiparasite association Acacia gerrardiiViscum schimperi. The hemiparasite exhibited 2.4- and 3.0-fold lower photosynthetic activity and water use efficiency, and 1.2- and 4.1-fold higher transpiration rate and stomatal conductance. Equally, it displayed 4.9- and 2.6-fold greater water potential and osmotic potential, and in least 3.0 times more accumulated 39K, 85Rb and 51V, compared to the host. Nevertheless, it had no detrimental effect on photosynthetic activity, water status and multi-element accumulations in the host. Based on metabolome profiling, V. schimperi could use xanthurenic acid and propylparaben to acquire potassium from the host, and N-1-naphthylacetamide and N-Boc-hydroxylamine to weaken or kill the distal part of the infected branch and to receive the total xylem contents. In contrast, A. gerrardii could used N-acetylserotonin, arecoline, acetophenone and 6-methoxymellein to defend against V. schimperi infection.

Keywords: Acacia gerrardii, multi-elements, osmotic potential, parasitism, photosynthesis, untargeted metabolites, Viscum schimperi, water potential.

References

Ackroyd RD, Graves JD (1997) The regulation of the water potential gradient in the host and parasite relationship between Sorghum bicolor and Striga hermonthica. Annals of Botany 80, 649-656.
| Crossref | Google Scholar |

Aihemaiti A, Gao Y, Meng Y, Chen X, Liu J, Xiang H, Xu Y, Jiang J (2020) Review of plant-vanadium physiological interactions, bioaccumulation, and bioremediation of vanadium-contaminated sites. Science of The Total Environment 712, 135637.
| Crossref | Google Scholar | PubMed |

Ali B, Mwamba TM, Gill RA, Yang C, Ali S, Daud MK, Wu Y, Zhou W (2014) Improvement of element uptake and antioxidative defense in Brassica napus under lead stress by application of hydrogen sulfide. Plant Growth Regulation 74, 261-273.
| Crossref | Google Scholar |

Aly R, Hamamouch N, Abu-Nassar J, Wolf S, Joel DM, Eizenberg H, Kaisler E, Cramer C, Gal-On A, Westwood JH (2011) Movement of protein and macromolecules between host plants and the parasitic weed Phelipanche aegyptiaca Pers. Plant Cell Reports 30, 2233-2241.
| Crossref | Google Scholar | PubMed |

Anselmo-Moreira F, Teixeira-Costa L, Ceccantini G, Furlan CM (2019) Mistletoe effects on the host tree Tapirira guianensis: insights from primary and secondary metabolites. Chemoecology 29, 11-24.
| Crossref | Google Scholar |

Bredin J, Davin-Régli A, Pagès J-M (2005) Propyl paraben induces potassium efflux in Escherichia coli. Journal of Antimicrobial Chemotherapy 55, 1013-1015.
| Crossref | Google Scholar | PubMed |

Cameron DD, Geniez J-M, Seel WE, Irving LJ (2008) Suppression of host photosynthesis by the parasitic plant Rhinanthus minor. Annals of Botany 101, 573-578.
| Crossref | Google Scholar | PubMed |

Cimminoa A, Masia M, Rubialesb M, Evidentea A, Fernández-Apariciob M (2018) Allelopathy for parasitic plant management. Natural Product Communications 13, 289-294.
| Google Scholar |

Delvas N, Bauce E, Labbé C, Ollevier T, Bélanger R (2011) Phenolic compounds that confer resistance to spruce budworm. Entomologia Experimentalis et Applicata 141, 35-44.
| Crossref | Google Scholar |

Dobbertin M, Rigling A (2006) Pine mistletoe (Viscum album ssp. austriacum) contributes to Scots pine (Pinus sylvestris) mortality in the Rhone valley of Switzerland. Forest Pathology 36, 309-322.
| Crossref | Google Scholar |

Dräxl S, Müller J, Li WB, Michalke B, Scherb H, Hense BA, Tschiersch J, Kanter U, Schäffner AR (2013) Caesium accumulation in yeast and plants is selectively repressed by loss of the SNARE Sec22p/SEC22. Nature Communications 4, 2092.
| Crossref | Google Scholar | PubMed |

Ehleringer JR, Marshall JD (1995) Water relations. In ‘Parasitic plants’. (Eds MC Press, JD Graves) pp. 125–140. (Chapman and Hall: London, UK)

Ehleringer JR, Schulze E-D (1985) Mineral concentrations in an autoparasitic Phoradendron californicum growing on a parasitic P. californicum and its host, Cercidium floridum. American Journal of Botany 72, 568-571.
| Crossref | Google Scholar |

Escher P, Rennenberg H (2006) Influx of double labelled glutamine into mistletoes (Viscum album) from the xylem sap of its host (Abies alba). Plant Physiology and Biochemistry 44, 880-884.
| Crossref | Google Scholar | PubMed |

Escher P, Peuke AD, Bannister P, Fink S, Hartung W, Jiang F, Rennenberg H (2008) Transpiration, CO2 assimilation, WUE, and stomatal aperture in leaves of Viscum album (L.): effect of abscisic acid (ABA) in the xylem sap of its host (Populus x euamericana). Plant Physiology and Biochemistry 46, 64-70.
| Crossref | Google Scholar | PubMed |

Fahmy GM (2013) Ecophysiology of the holoparasitic angiosperm Cistanche phelypaea (Orobancaceae) in a coastal salt marsh. Turkish Journal of Botany 37, 908-919.
| Crossref | Google Scholar |

Glatzel G (1983) Mineral nutrition and water relations of hemiparasitic mistletoes: a question of partitioning. Experiments with Loranthus europaeus on Quercus petraea and Quercus robur. Oecologia 56, 193-201.
| Crossref | Google Scholar | PubMed |

Glatzel G, Geils BW (2009) Mistletoe ecophysiology: host–parasite interactions. Botany 87, 10-15.
| Google Scholar |

Graves JD, Wylde A, Press MC, Stewart GR (1990) Growth and carbon allocation in Pennisetum typhoides infected with the parasitic angiosperm Striga hermonthica. Plant, Cell & Environment 13, 367-373.
| Crossref | Google Scholar |

Hegenauer V, Körner M, Albert M (2017) Plants under stress by parasitic plants. Current Opinion in Plant Biology 38, 34-41.
| Crossref | Google Scholar | PubMed |

Heide-Jørgensen H (2008) ‘Parasitic flowering plants.’ (Brill Publishers: Leiden, Netherlands)

Hibberd JM, Bungard RA, Press MC, Jeschke WD, Scholes JD, Quick WP (1998) Localization of photosynthetic metabolism in the parasitic angiosperm Cuscuta reflexa. Planta 205, 506-513.
| Crossref | Google Scholar |

Irving LJ, Cameron DD (2009) You are what you eat: interactions between root parasitic plants and their hosts. Advances in Botanical Research 50, 87-138.
| Google Scholar |

Kim G, Westwood JH (2015) Macromolecule exchange in Cuscuta–host plant interactions. Current Opinion in Plant Biology 26, 20-25.
| Crossref | Google Scholar | PubMed |

Lamara M, Parent GJ, Giguère I, Beaulieu J, Bousquet J, Mackay JJ (2018) Association genetics of acetophenone defence against spruce budworm in mature white spruce. BMC Plant Biology 18, 231.
| Crossref | Google Scholar | PubMed |

Leigh RA (2001) Potassium homeostasis and membrane transport. Journal of plant Nutrition and Soil Science 164, 193-198.
| Crossref | Google Scholar |

Llugany M, Lombini A, Dinelli E, Poschenrieder C, Barcelo J (2009) Transfer of selected mineral nutrients and trace elements in the host–hemiparasite association, Cistus Odontites lutea, growing on and off metal-polluted sites. Plant Biology 11, 170-178.
| Crossref | Google Scholar | PubMed |

Lüttge U (2008) ‘Physiological ecology of tropical plants.’ 2nd edn. (Springer: Berlin, Germany)

Machado MA, Zetsche K (1990) A structural, functional and molecular analysis of plastids of the holoparasites Cuscuta reflexa and Cuscuta europaea. Planta 181, 91-96.
| Crossref | Google Scholar | PubMed |

Maes WH, Huete AR, Avino M, Boer MM, Dehaan R, Pendall E, Griebel A, Steppe K (2018) Can UAV-based infrared thermography be used to study plant-parasite interactions between mistletoe and eucalypt trees? Remote Sensing 10, 2062.
| Crossref | Google Scholar |

Marschner H (1995) ‘Mineral nutrition of higher plants.’ 2nd edn. (Academic Press: London, UK)

Marshall JD, Ehleringer JR (1990) Are xylem-tapping mistletoes partially heterotrophic? Oecologia 84, 244-248.
| Crossref | Google Scholar | PubMed |

Maul K, Krug M, Nickrent DL, Müller KF, Quandt D, Wicke S (2019) Morphology, geographic distribution, and host preferences are poor predictors of phylogenetic relatedness in the mistletoe genus Viscum L. Molecular Phylogenetics and Evolution 131, 106-115.
| Crossref | Google Scholar | PubMed |

Murtaza G, Javed W, Hussain A, Wahid A, Murtaza B, Owens G (2015) Metal uptake via phosphate fertilizer and city sewage in cereal and legume crops in Zea mays Pakistan. Environmental Science and Pollution Research 22, 9136-9147.
| Crossref | Google Scholar | PubMed |

Mutlu S, Atici O, Esim N, Mete E (2011) Essential oils of catmint (Nepeta meyeri Benth.) induce oxidative stress in early seedlings of various weed species. Acta Physiologiae Plantarum 33, 943-951.
| Crossref | Google Scholar |

Mutlu S, Osma E, Ilhan V, Turkoglu HI, Atici O (2016) Mistletoe (Viscum album) reduces the growth of the Scots pine by accumulating essential nutrient elements in its structure as a trap. Trees 30, 815-824.
| Crossref | Google Scholar |

Nyholm NEI, Tyler G (2000) Rubidium content of plants, fungi and animals closely reflects potassium and acidity conditions of forest soils. Forest Ecology and Management 134, 89-96.
| Crossref | Google Scholar |

Pennings SC, Callaway RM (2002) Parasitic plants: parallels and contrasts with herbivores. Oecologia 131, 479-489.
| Crossref | Google Scholar | PubMed |

Press MC (1998) Dracula or Robin Hood? A functional role for root hemiparasites in nutrient poor ecosystems. Oikos 82, 609-611.
| Crossref | Google Scholar |

Press MC, Phoenix GK (2005) Impacts of parasitic plants on natural communities. New Phytologist 166, 737-751.
| Crossref | Google Scholar | PubMed |

Press MC, Whittaker JB (1993) Exploitation of the xylem stream by parasitic organisms. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 341, 101-111.
| Crossref | Google Scholar |

Press MC, Graves JD, Stewart GR (1990) Physiology of the interaction of angiosperm parasites and their higher plant hosts. Plant, Cell & Environment 13, 91-104.
| Crossref | Google Scholar |

Rahman R, Upadhyaya H (2021) Aluminium toxicity and its tolerance in plant: a review. Journal of Plant Biology 64, 101-121.
| Crossref | Google Scholar |

Raju M, Patel TJ, Nair RR, Chatterjee PB (2016) Xanthurenic acid: a natural ionophore with high selectivity and sensitivity for potassium ions in an aqueous solution. New Journal of Chemistry 40, 1930-1934.
| Crossref | Google Scholar |

Reid N, Yan ZG, Fittler J (1994) Impact of mistletoes (Amyema miquelii) on host (Eucalyptus blakelyi and Eucalyptus melliodora) survival and growth in temperate Australia. Forest Ecology and Management 70, 55-65.
| Crossref | Google Scholar |

Rizwan M, Ali S, Abbas T, Zia-ur-Rehman M, Hannan F, Keller C, Al-Wabel MI, Ok YS (2016) Cadmium minimization in wheat: a critical review. Ecotoxicology and Environmental Safety 130, 43-53.
| Crossref | Google Scholar | PubMed |

Scalon MC, Rossatto DR, Domingos FMCB, Franco AC (2016) Leaf morphophysiology of a neotropical mistletoe is shaped by seasonal patterns of host leaf phenology. Oecologia 180, 1103-1112.
| Crossref | Google Scholar | PubMed |

Seneviratne M, Rajakaruna N, Rizwan M, Madawala HMSP, Ok YS, Vithanage M (2019) Heavy metal-induced oxidative stress on seed germination and seedling development: a critical review. Environmental Geochemistry and Health 41, 1813-1831.
| Crossref | Google Scholar | PubMed |

Shen H, Ye W, Hong L, Huang H, Wang Z, Deng X, Yang Q, Xu Z (2006) Progress in parasitic plant biology: host selection and nutrient transfer. Plant Biology 8, 175-185.
| Crossref | Google Scholar | PubMed |

Singh RP, Tripathi RD, Sinha SK, Maheshwari R, Srivastava HS (1997) Response of higher plants to lead contaminated environment. Chemosphere 34, 2467-2493.
| Crossref | Google Scholar | PubMed |

Smith S, Stewart GR (1990) Effect of potassium levels on the stomatal behavior of the hemi-parasite Striga hermonthica. Plant Physiology 94, 1472-1476.
| Crossref | Google Scholar | PubMed |

Strong GL, Bannister P, Burritt D (2000) Are mistletoes shade plants? CO2 assimilation and chlorophyll fluorescence of temperate mistletoes and their hosts. Annals of Botany 85, 511-519.
| Crossref | Google Scholar |

Tsopelas P, Angelopoulos A, Economou A, Soulioti N (2004) Mistletoe (Viscum album) in the fir forest of Mount Parnis, Greece. Forest Ecology and Management 202, 59-65.
| Crossref | Google Scholar |

Türe C, Böcük H, Asan Z (2010) Nutritional relationships between hemi-parasitic mistletoe and some of its deciduous hosts in different habitats. Biologia 65, 859-867.
| Crossref | Google Scholar |

Těšitel J (2016) Functional biology of parasitic plants: a review. Plant Ecology and Evolution 149, 5-20.
| Crossref | Google Scholar |

Těšitel J, Těšitelová T, Fisher JP, Lepš J, Cameron DD (2015) Integrating ecology and physiology of root-hemiparasitic interaction: interactive effects of abiotic resources shape the interplay between parasitism and autotrophy. New Phytologist 205, 350-360.
| Crossref | Google Scholar | PubMed |

Těšitel J, Li A-R, Knotkováa K, McLellan R, Bandaranayake PCG, Watson DM (2021) The bright side of parasitic plants: what are they good for? Plant Physiology 185, 1309-1324.
| Crossref | Google Scholar |

Varga I, Taller J, Baltazar T, Hyvonen J, Poczai P (2012) Leaf-spot disease on European mistletoe (Viscum album) caused by Phaeobotryosphaeria visci: a potential candidate for biological control. Biotechnology Letters 34, 1059-1065.
| Crossref | Google Scholar | PubMed |

Walters DR (2011) ‘Plant defense: warding off attack by pathogens, herbivores, and parasitic plants.’ (Wiley-Blackwell: Oxford, UK)

Watling JR, Press MC (2001) Impacts of infection by parasitic angiosperms on host photosynthesis. Plant Biology 3, 244-250.
| Crossref | Google Scholar |

Westwood JH, Yoder JI, Timko MP, de Pamphilis CW (2010) The evolution of parasitism in plants. Trends in Plant Science 15, 227-235.
| Crossref | Google Scholar | PubMed |

White PJ, Wiesel L, Broadley MR (2010) Cation channels and the uptake of radiocaesium by plants. In ‘Ion channels and plant stress responses. Signaling and Communication in Plants’. (Eds V Demidchik, F Maathuis) pp. 47–67. (Springer-Verlag: Berlin, Heidelberg, Germany)

Yang Z, Wafula EK, Honaas LA, et al. (2015) Comparative transcriptome analyses reveal core parasitism genes and suggest gene duplication and repurposing as sources of structural novelty. Molecular Biology and Evolution 32, 767-790.
| Crossref | Google Scholar | PubMed |

Yao J-W, Ma Z, Ma Y-Q, Zhu Y, Lei M-Q, Hao C-Y, Chen L-Y, Xu Z-Q, Huang X (2021) Role of melatonin in UV-B signaling pathway and UV-B stress resistance in Arabidopsis thaliana. Plant, Cell & Environment 44, 114-129.
| Crossref | Google Scholar | PubMed |

Yin X, Wei Y, Song W, Zhang H, Liu G, Chen Y, Li L-Z, Alolga RN, Ma G, Reiter RJ, Li J, Shi H (2020) Melatonin as an inducer of arecoline and their coordinated roles in anti-oxidative activity and immune responses. Food & Function 11, 8788-8799.
| Crossref | Google Scholar | PubMed |

Zagorchev L, Stöggl W, Teofanova D, Li J, Kranner I (2021) Plant parasites under pressure: effects of abiotic stress on the interactions between parasitic plants and their hosts. International Journal of Molecular Sciences 22, 7418.
| Crossref | Google Scholar | PubMed |

Zahra N, Hafeez MB, Shaukat K, Wahid A, Hasanuzzaman M (2021) Fe toxicity in plants: impacts and remediation. Physiologia Plantarum 173, 201-222.
| Crossref | Google Scholar | PubMed |

Zhao D, Wang H, Chen S, Yu D, Reiter RJ (2021) Phytomelatonin: an emerging regulator of plant biotic stress resistance. Trends in Plant Science 26, 70-82.
| Crossref | Google Scholar | PubMed |

Zhu Y, Guo M-J, Song J-B, Zhang S-Y, Guo R, Hou D-R, HAo C-Y, An H-L, Huang X (2021) Roles of endogenous melatonin in resistance to Botrytis cinerea infection in an Arabidopsis model. Frontiers in Plan Science 12, 683228.
| Crossref | Google Scholar |