Abstract
Seedlings of parasitic Cuscuta species are autotrophic but can survive only a short period of time, during which they must locate and attach to a suitable host. They have an ephemeral root-like organ considered not a “true” root by most studies. In the present study, two species with contrasting ecology were examined: Cuscuta gronovii, a North American riparian species, and Cuscuta campestris, an invasive dodder that thrives in disturbed habitats. The morphology, structure, and absorptive capability of their root-like organ were compared, their potential for colonization by two species of arbuscular mycorrhizal fungi (AMF) was assessed, and the effect of the AMF on seedling growth and survival was determined. The root of both species absorbed water and interacted with AMF, but the two species exhibited dissimilar growth and survival patterns depending on the colonization level of their seedlings. The extensively colonized seedlings of C. gronovii grew more and survived longer than non-colonized seedlings. In contrast, the scarce colonization of C. campestris seedlings did not increase their growth or longevity. The differential growth responses of the AMF-colonized and non-colonized Cuscuta species suggest a mycorrhizal relationship and reflect their ecology. While C. gronovii roots have retained a higher ability to interact with AMF and are likely to take advantage of fungal communities in riparian habitats, the invasive C. campestris has largely lost this ability possibly as an adaptation to disturbed ecosystems. These results indicate that dodders have a true root, even if much reduced and ephemeral, that can interact with AMF.
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References
Albert M, Kaiser B, van der Krol S, Kaldenhoff R (2010) Calcium signaling during the plant-plant interaction of parasitic Cuscuta reflexa with its hosts. Plant Signal Behav 5:1144–1146
Allen MF (1991) The ecology of mycorrhizae. Cambridge University Press, New York
Bécard G, Fortin JA (1988) Early events of vesicular-arbuscular mycorrhizal formation on Ri T-DNA transformed roots. New Phytol 118:211–218
Braukmann T, Kuzmania M, Stefanović S (2013) Plastid genome evolution across the genus Cuscuta (Convolvulaceae): two clades within subgenus Grammica exhibit extensive gene loss. J Exp Bot 64:977–989
Brundrett MC (2011) Commentary on the de Vega et al. (2010) paper on hyphae in the parasitic plant Cytinus: mycorrhizal fungi growing within plants are not always mycorrhizal. Am J Bot 98:595–596
Costea M, Stefanović S (2009) Cuscuta jepsonii (Convolvulaceae): an invasive weed or an extinct endemic? Am J Bot 96:1744–1750
Costea M, Tardif FJ (2006) The biology of Canadian weeds. 133. Cuscuta campestris Yuncker, Cuscuta gronovii Willd.ex schult., Cuscuta umbrosa Beyr. Ex Hook., Cuscuta epithymum(L) L. and Cuscuta epilinum Weihe. Can J Pl Sci 86:293–316
Costea M, Nesom GL, Stefanović S (2006a) Taxonomy of Cuscuta gronovii and Cuscuta umbrosa (Convolvulaceae). Sida 22:197–207
Costea M, Nesom GL, Stefanović S (2006b) Taxonomy of Cuscuta pentagona complex (Convolvulaceae) in North America. Sida 22:151–175
Costea M, García M, Stefanović S (2015) A phylogenetically based infrageneric classification of parasitic plant genus Cuscuta (dodders, Convolvulaceae). Syst Bot 40
Dawson JH, Musselman LJ, Wolswinkel P, Dörr I (1994) Biology and control of Cuscuta. Rev Weed Sci 6:265–317
De Long JR, Swarts ND, Dixon KW, Egerton-Warburton LM (2013) Mycorrhizal preference promotes habitat invasion by a native Australian orchid: Microtis media. Ann Bot 111:409–418
de Vega C, Arsita M, Ortiz PL, Talavera S (2010) Anatomical relations among endophytic holoparasitic angiosperms, autotrophic host plants and mycorrhizal fungi: a novel tripartite interaction. Am J Bot 97:730–737
de Vega C, Arista M, Ortiz PL, Talavera S (2011) Mycorrhizal fungi and parasitic plants: reply. Am J Bot 98:597–601
Dubrovsky JG, Guttenberger M, Saralegui A, Napsucialy-Medivil S, Voigt B, Baluška F, Menzel D (2006) Neutral red as a probe for confocal laser scanning microscopy studies of plant roots. Ann Bot 97:127–1138
Flury M, Flühler H (1995) Tracer characteristics of brilliant blue FCF. Soil Sci Soc Am J 59:22–27
García J, Barker DG, Journet EP (2006) Seed storage and germination. In: Mathesius U (ed) The Medicago truncatula handbook. The Samuel Roberts Noble Foundation, Ardmore http://www.noble.org/MedicagoHandbook/
García MA, Costea M, Kuzmina M, Stefanović S (2014) Phylogeny, character evolution and biogeography of Cuscuta (dodders, Convolvulaceae) inferred from coding plastid and nuclear sequences. Am J Bot 101:1–21
Grubb PJ (1977) The maintenance of species richness in plant communities: the importance of the regeneration niche. Biol Rev 52:107–145
Guinel F, Hirsch AM (2000) The involvement of root hairs in mycorrhizal associations. In: Ridge RW, Emos AMC (eds) Cell and molecular biology of plant root hairs. Springer, Berlin, pp 285–310
Gutjahr C (2014) Phytohormone signaling in arbuscular mycorrhiza development. Curr Opin Plant Biol 20:26–34
Haccius B, Troll W (1961) Über die sogennanten Wurtzelhaare an den Keimpflanzen von Drosera—und Cuscuta arten. Beitr Biol Pfl 36:139–157
Harper JL (1977) Population biology of plants. Academic, London
Heide-Jorgensen HS (2008) Parasitic flowering plants. Brill, Boston
Hempel S, Goetzenberger L, Kuehn I, Michalski SG, Rillig MC, Zobel M, Moora M (2013) Mycorrhizas in the Central European flora: relationships with plant life history traits and ecology. Ecology 94:1389–1399
Hibberd JM, Bungard RM, Press MC, Jeschke WD, Scholes JD, Quick WP (1998) Localization of photosynthetic metabolism in the parasitic angiosperm Cuscuta reflexa. Planta 205:506–513
Holm L, Doll J, Holm E, Pancho J, Herberger J (1997) World weeds: natural histories and distribution. Wiley, Toronto
Isselstein J, Tallowin JRB, Smith REN (2002) Factors affecting seed germination and seedling establishment of fen‐meadow species. Restor Ecol 10:173–184
Kaufmann K, Pajoro A, Angenent GC (2010) Regulation of transcription in plants: mechanisms controlling developmental switches. Nat Rev Genet 11:830–842
Khalid AN, Iqbal SH (1996) Mycotrophy in a vascular stem parasite Cuscuta reflexa. Mycorrhiza 6:69–71
Koch L (1880) Die Klee-und flachsseide (Cuscuta epithymum und C. epilinum): untersuchungen über deren entwicklung verbreitung und vertilgung. Carl Winters Universitätsbuchhandlung, Heidelberg
Koide RT, Mosse B (2004) A history of research on arbuscular mycorrhiza. Mycorrhiza 14:145–163
Krause K (2008) From chloroplasts to ‘cryptic’ plastids: evolution of plastid genomes in parasitic plants. Curr Genet 54:111–121
Krüger M, Keruger C, Walker C, Stockinger H, Schüβler A (2012) Phylogenetic reference data for systematic and phylotaxonomy of arbuscular mycorrhizal fungi from phylum to species level. New Phytol 193:970–984
Lanini WT, Kogan M (2005) Biology and management of Cuscuta in crops. Cienc Investig Agrar 32:127–141
Lee KB, Park JB, Lee S (2000) Morphology and anatomy of mature embryos and seedlings in parasitic angiosperm Cuscuta japonica. J Plant Biol 43:22–27
Lee KJ, Eom AH, Lee SS (2002) Multiple symbiotic associations found in the roots of Botrychium ternatum. Microbiology 30:164–153
Li AR, Guan KY (2008) Arbuscular mycorrhizal fungi may serve as another nutrient strategy for some hemiparasitic species of Pedicularis (Orobanchaceae). Mycorrhiza 18:429–436
Li AR, Guan KY, Stonor R, Smith SE, Smith FA (2013) Direct and indirect influences of arbuscular mycorrhizal fungi on phosphorus uptake by two root hemiparasitic Pedicularis species: do the fungal partners matter at low colonization levels? Ann Bot 112:1089–1098
Lyshede OB (1985) Morphological and anatomical features of Cuscuta pedicellata and C. campestris. Nord J Bot 5:65–77
Lyshede OB (1986) Fine structural features of the tuberous radicular end of the seedling of Cuscuta pedicellata. Ber Deut Bot Ges 99:105–109
Lyshede OB (1989) Microscopy of filiform seedling axis of Cuscuta pedicellata. Bot Gaz 150:230–238
Ma F, Peterson CA (2000) Plasmodesmata in onion (Allium cepa L.) roots: a study enabled by improved fixation and embedding techniques. Protoplasma 211:103–115
Mader JC, Turnbull CGN, Emery RJ (2003) Transport and metabolism of xylem cytokinins during lateral bud release in decapitated chickpea (Cicer arietinum) seedlings. Physiol Plant 117:118–129
Maestre FT, Cortina J, Bautista S, Bellot J, Vallejo R (2003) Small-scale environmental heterogeneity and spatiotemporal dynamics of seedling establishment in a semiarid degraded ecosystem. Ecosystems 6:630–643
Marambe B, Wijesundara S, Tennakoon K, Pindeiya D, Jayasinghe C (2002) Growth and development of Cuscuta chinensis Lam. and its impact on selected crops. Weed Biol Manag 2:79–83
Maun MA (1994) Adaptations enhancing survival and establishment of seedlings on coastal dune systems. Vegetatio 111:59–70
Novero M, Genre A, Szczyglowski K, Bonfante P (2009) Root hair colonization by mycorrhizal fungi. In: Emons AMC, Ketelaar T (eds) Root hairs. Plant Cell Monographs 12:315–338
O’Brien TP, McCully ME (1981) The study of plant structure: principles and selected methods. Termarcarphi Pty. Ltd, Melbourne
Oldroyd GED (2013) Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Microbiology 11:252–263
Parker C, Riches C (1993) Parasitic weeds of the world: biology and control. CAB International, Wallingford
Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6:763–775
Peterson RL, Massicotte HB, Melville LH (2003) Mycorrhizas: anatomy and cell biology. NRC Research Press, Ottawa
Press MC, Phoenix GK (2005) Impacts of parasitic plants on natural communities. New Phytol 166:737–751
Pringle A, Bever JD, Gardes M, Parrent JL, Rillig MC, Klironomos JN (2009) Mycorrhizal symbioses and plant invasions. Annu Rev Ecol Evol S 40:699–715
Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212
Runyon JB, Mescher MC, De Moraes CM (2006) Volatile chemical cues guide host location and host selection by parasitic plants. Science 313:1964–1967
Sandler HA (2010) Managing Cuscuta gronovii (swamp dodder) in cranberry requires an integrated approach. Sustainability 2:660–683
Sherman TD, Bowling AJ, Barger TW, Vaughn KC (2008) The vestigial root of dodder (Cuscuta pentagona) seedlings. Int J Plant Sci 169:998–1012
Taylor DL, Bruns TD, Hodges SA (2004) Evidence for mycorrhizal races in a cheating orchid. Proc Royal Soc London B Biol 271:35–43
Timmers ACJ, Tirlapur UK, Schel JHN (1995) Vacuolar accumulation of acridine orange and neutral red in zygotic and somatic embryos of carrot (Daucus carota L.). Protoplasma 146:133–142
Truscott FH (1966) Some aspect of morphogenesis in Cuscuta gronovii. Am J Bot 53:739–750
Veiga RS, Faccio A, Genre A, Pieterse CM, Bonfante P, Heijden MG (2013) Arbuscular mycorrhizal fungi reduce growth and infect roots of the non‐host plant Arabidopsis thaliana. Plant Cell Environ 36:1926–1937
Vierheilig H, Coughlan AP, Wyss U, Piché Y (1998) Ink-vinegar, a sample staining technique for arbuscular mycorrhizal fungi. Appl Environ Microb 64:5004–5007
Wolf JB (2013) Principles of transcriptome analysis and gene expression quantification: an RNA‐seq tutorial. Mol Ecol Resour 13:559–572
Yuncker TG (1932) The genus Cuscuta. Mem Torrey Bot Club 18:113–331
Acknowledgments
We are grateful to Kevin Stevens for the help with the fungal scoring technique in the small roots of Cuscuta and to Susan Belfry from UNB, Microscopy and Microanalysis Facility for the assistance with the TEM. We also thank Larry Peterson and Kevin Stevens for providing constructive comments on an earlier draft of the manuscript. Two reviewers provided valuable suggestions that improved the manuscript. This research was supported by a Discovery grant from Natural Sciences and Engineering Research Council (NSERC) of Canada (327013–06) and by Wilfrid Laurier University (240329) to M. Costea.
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Fig. S1
Transmission electron microscopy of putative root cap cells from 1-day-old seedlings of Cuscuta gronovii. (a) View of several cells, alive with dense cytoplasm. (b) Cell walls are thick, pectinaceous; numerous lipid droplets (l) are present in certain cells while other cells display numerous mitochondria (m). (c) Abundant smooth endoplasmic reticulum (ser) suggesting active lipid biosynthesis. (d). The lipid droplets (l) appear to aggregate into larger structures. (e–f) Plastids (amyloplasts, p) are also common in cells. (GIF 514 kb)
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Behdarvandi, B., Guinel, F.C. & Costea, M. Differential effects of ephemeral colonization by arbuscular mycorrhizal fungi in two Cuscuta species with different ecology. Mycorrhiza 25, 573–585 (2015). https://doi.org/10.1007/s00572-015-0632-9
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DOI: https://doi.org/10.1007/s00572-015-0632-9