Hemiparasitic interaction between Castilleja tenuiflora (Orobanchaceae) and Baccharis conferta (Asteraceae): haustorium anatomy and C- and N-fluxes

keywords: C-, N- and chrolophyll levels, endophyte, essential oils, haustorium, hemiparasitism, parasitic plants


Background: Castilleja tenuiflora is a hemiparasite of Baccharis conferta. The haustorium is the characteristic structure of hemiparasitic plants and its anatomy varies depending several factors such as host species, position on the root and environment.

Question: What is the structure and anatomy of haustoria builded in field interaction? Based on C, N and chlorophyll contents, is C. tenuiflora a facultative hemiparasite of B. conferta?

Species studied: Castilleja tenuiflora Benth. and Baccharis conferta Kunth.

Study site and dates: Plant materials were collected in the Iztaccihuatl-Popocatepetl National Park (N 19° 0.5´ 9.6'', W 98° 40´ 24.2'', 3,480 m.a.s.l.), State of Mexico, Mexico, in December 2013.

Methods: Individuals of B. conferta and C. tenuiflora growing independently or in hemiparasite interactions were collected and samples were processed for anatomical and histochemical characterization, determination of C, N and chlorophyll.

Results: Haustoria were globular and located mainly in the lateral roots of B. conferta. Anatomy of haustorium shows the characteristic structures: exophyte and endophyte. Haustorial tissues storage starch, tannins and essential oils while in the B. conferta roots also calcium oxalate crystals were found. C levels were significantly influenced by hemiparasitic interaction. This is the first study that characterizes a hemiparasitic interaction in the field and specifically between C. tenuiflora and B. conferta.

Conclusions: Haustoria builded in interaction with B. conferta show the characteristic structure and anatomy. Hemiparasitic relationship represents for C. tenuiflora a source of C and other compounds such as essential oils.


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Hemiparasitic interaction between <em>Castilleja tenuiflora</em> (Orobanchaceae) and <em>Baccharis conferta</em> (Asteraceae): haustorium anatomy and C- and N-fluxes


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 Rep 30 (12): 2233-2241. DOI:10.1007/s00299-011-1128-5

Barbieri Xavier V, Vargas RMF, Minteguiaga M, Umpiérrez N, Dellacassa E, Cassel E. 2013. Evaluation of the key odorants of Baccharis anomala DC essential oil: New applications for known products. Industrial Crops and Products 49: 492-496. DOI:10.1016/j.indcrop.2013.05.011

Bobek VB, Heiden G, de Oliveira CF, de Almeida VP, de Paula JP, Farago PV, Nakashima T, Budel JM. 2016. Comparative analytical micrographs of “vassouras” (Baccharis, Asteraceae). Brazilian Journal of Pharmacognosy 26: 665-672. DOI:10.1016/j.bjp.2016.05.001

Cameron DD, Seel WE. 2007. Functional anatomy of haustoria formed by Rhinanthus minor: linking evidence from histology and isotope tracing. New Phytologist 174: 412-419. DOI:10.1111/j.1469-8137.2007.02013.x

Cechin I, Press MC. 1993. Nitrogen relations of the sorghum-Striga hermonthica host-parasite association: germination, attachment and early growth. New Phytologist 124: 681-687. DOI:10.1111/j.1469-8137.1993.tb03858.x

Dobbins DR, Kuijt J. 1973. Studies on haustorium of Castilleja (Scrophulariaceae) .1. Upper haustorium. Canadian Journal of Botany 51: 917-922

Espírito-Santo M, Wilson Fernandes G, Allain L, Reis T. 1999. Tannins in Baccharis dracunculifolia (Asteraceae): effects of seasonality, water availability and plant sex. Acta Botanica Brasilica 13: 167-174

Estabrook E, Yoder JI. 1998. Plant-Plant communications: Rhizosphere signaling between parasitic angiosperms and their hosts. Plant Physiology 116: 1-7

Furlan CM, Barbosa L, Alves DY 2011 Tannins: what do they represent in plant life? In: Petridis GK (ed) Tannins: types, foods containing and nutrition. Nova Science Publishers, Inc., New York, pp 251-263

Furuhashi T, Nakamura T, Iwase K. 2016. Analysis of metabolites in stem parasitic plant interactions: Interaction of Cuscuta-Momordica versus Cassytha-Ipomoea. Plants 5: 43. DOI:10.3390/plants5040043

Herrera-Ruiz M, López-Rodríguez R, Trejo-Tapia G, Domínguez-Mendoza B, González-Cortazar M, Tortoriello J, Zamilpa A. 2015. A new furofuran lignan diglycoside and other secondary metabolites from the antidepressant extract of Castilleja tenuiflora Benth. Molecules 20: 13127-13143. DOI:10.3390/molecules200713127

Irving LJ, Cameron DD 2009 You are what you eat: Interactions between root parasitic plants and their hosts. In: Jean-Claude K, Michel D (eds) Advances in Botanical Research, vol 50. Academic Press, pp 87-138. doi:10.1016/S0065-2296(08)00803-3

Jasinski VCG, da Silva RZ, Pontarolo R, Budel JM, Campos FR. 2014. Morpho-anatomical characteristics of Baccharis glaziovii in support of its pharmacobotany. Brazilian Journal of Pharmacognosy 24: 609-616. DOI:10.1016/j.bjp.2014.11.003

Joel DM 2013 Functional structure of the mature haustorium. In: Joel DM, Gressel J, Musselman LJ (eds) Parasitic Orobanchacea. Parasitic mechanisms and control strategies. Spriger-Verlag, London, pp 25-60. doi:10.1007/978-3-642-38146-1_16

Kartal C. 2016. Calcium oxalate crystals in some species of the Tribe Cardueae (Asteraceae). Botanical Sciences 94 (1). DOI:10.17129/botsci.259

Kim G, Westwood JH. 2015. Macromolecule exchange in Cuscuta-host plant interactions. Current Opinion in Plant Biology 26: 20-25. DOI:10.1016/j.pbi.2015.05.012

Lago JHG, Romoff P, Fávero OA, Souza FO, Soares MG, Baraldi PT, Corrêa AG. 2008. Chemical composition of male and female Baccharis trimera (Less.) DC. (Asteraceae) essential oils. Biochemical Systematics and Ecology 36: 737-740. DOI:10.1016/j.bse.2008.05.009

Lichtenthaler HK 1987 Chlorophylls and carotenoids: Pigments of photosynthetic biomembranes. In: Lester Packer RD (ed) Methods in Enzymology, vol Volume 148. Academic Press, pp 350-382. doi:10.1016/0076-6879(87)48036-1

Luo FL, Guo QS. 2010. Influences of host species on transpiration, photosynthesis, chlorophyll and mineral contents of medicinal hemiparasite Thesium chinense Turcz. Acta Physiologiae Plantarum 32 (6): 1093-1102. DOI:10.1007/s11738-010-0501-2

Marshall J, Ehleringer J. 1990. Are xylem-tapping mistletoes partially heterotrophie? Oecologia 84: 244-248

Marvier MA. 1996. Parasitic plant-host interactions: Plant performance and indirect effects on parasite-feeding herbivores. Ecology 77: 1398-1409

Montes-Hernández E, Sandoval-Zapotitla E, Bermúdez-Torres K, Trejo-Tapia G. 2015. Potential hosts of Castilleja tenuiflora (Orobanchaceae) and characterization of its haustoria. Flora 214: 11-16. DOI:10.1016/j.flora.2015.05.003

Nakata PA. 2003. Advances in our understanding of calcium oxalate crystal formation and function in plants. Plant Science 164: 901-909. DOI:10.1016/s0168-9452(03)00120-1

Perera WH, Bizzo HR, Gama PE, Alviano CS, Salimena FRG, Alviano DS, Leitão SG. 2016. Essential oil constituents from high altitude Brazilian species with antimicrobial activity: Baccharis parvidentata Malag., Hyptis monticola Mart. ex Benth. and Lippia origanoides Kunth. Journal of Essential Oil Research 29: 109-116. DOI:10.1080/10412905.2016.1210039

Piehl MA. 1963. Mode of attachment, haustorium structure, and hosts of Pedicularis canadensis. American Journal of Botany 50: 978-985. DOI:10.2307/2439904

Press M, Shah N, Touhy J, Stewart G. 1987. Carbono isotope demostrate carbon flux from C4 host to C3 parasite. Plant Physiology 85: 1143-1145

Qing-Liang C, Ya-Min J, Zhi-Fen W, Cheng-Gang S, Jing-Bin Z, Yu-Hai G. 2011. Postembryonic development of Cistanche tubulosa (Schrenk) Whight. Pakistan Journal of Botany 43: 1823-1830

Rümer S, Cameron DD, Wacker R, Hartung W, Jiang F. 2007. An anatomical study of the haustoria of Rhinanthus minor attached to roots of different hosts. Flora 202: 194-200. DOI:10.1016/j.flora.2006.07.002

Salminen J-P, Karonen M. 2011. Chemical ecology of tannins and other phenolics: we need a change in approach. Functional Ecology 25: 325-338. DOI:10.1111/j.1365-2435.2010.01826.x

Sanchez PM, Villarreal ML, Herrera-Ruiz M, Zamilpa A, Jiménez-Ferrer E, Trejo-Tapia G. 2013. In vivo anti-inflammatory and anti-ulcerogenic activities of extracts from wild growing and in vitro plants of Castilleja tenuiflora Benth. (Orobanchaceae). Journal of Ethnopharmacology 150: 1032-1037. DOI:10.1016/j.jep.2013.10.002

Sandoval E, Rojas LA, Guzmán RC, Carmona JL, Ponce SRM, León GC, Loyola BC, Vallejo ZMA, Medina AA. 2005. Técnicas aplicadas al estudio de la anatomía vegetal. Universidad Nacional Autónoma de México, México, D. F.

Stitt M, Zeeman SC. 2012. Starch turnover: pathways, regulation and role in growth. Current Opinion in Plant Biology 15: 282-292. DOI:10.1016/j.pbi.2012.03.016

Tennakoon K, Pate J. 1996. Heterotrophic gain of carbon from hosts by the xylem- apping root hemiparasite Olax phyllanthi (Olacaceae). Oecologia 105: 369-376

Tesitel J, Leps J, Vrablova M, Cameron DD. 2011. The role of heterotrophic carbon acquisition by the hemiparasitic plant Rhinanthus alectorolophus in seedling establishment in natural communities: a physiological perspective. New Phytologist 192: 188-199. DOI:10.1111/j.1469-8137.2011.03777.x

Tesitel J, Plavcova L, Cameron DD. 2010a. Heterotrophic carbon gain by the root hemiparasites, Rhinanthus minor and Euphrasia rostkoviana (Orobanchaceae). Planta 231: 1137-1144. DOI:10.1007/s00425-010-1114-0

Tesitel J, Plavcova L, Cameron DD. 2010b. Interactions between hemiparasitic plants and their hosts: the importance of organic carbon transfer. Plant Signaling Behaviour 5: 1072-1076. DOI:10.4161/psb.5.9.12563

Tesitel J, Tesitelova T, Fisher JP, Leps 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 (1): 350-360. DOI:10.1111/nph.13006

Van Bel AJE. 1990. Xylem-Phloem Exchange Via the Rays: The Undervalued Route of Transport. Jounal of Experimental Botany 41: 631-644. DOI:10.1093/jxb/41.6.631

Vannini AB, Santos TG, Fleming AC, Purnhagen LRP, Lourenço LA, Butzke ETB, Kempt M, Begnini IM, Rebelo RA, Dalmarco EM, Bella Cruz A, Schmit AP, Cruz RCB, Yamanaka CN, Steindel M. 2012. Chemical characterization and antimicrobial evaluation of the essential oils from Baccharis uncinella D.C. and Baccharis semiserrata D.C. (Asteraceae). Journal of Essential Oil Research 24: 547-554. DOI:10.1080/10412905.2012.728092

Visser J, Dörr I, Kollmann R. 1984. The hyaline body of the root parasite Alectra orobanchoides Benth. (Scrophulariaceae)- its anatomy, ultraestructure and histochemistry. Protoplasma 121: 146-156

Watling J, Press M. 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 and Cell Environment 20: 1292-1300

Westwood JH 2013 The Physiology of the Established Parasite–Host Association. In: Joel DM, Gressel J, Musselman LJ (eds) Parasitic Orobanchaceae: Parasitic Mechanisms and Control Strategies. Springer Berlin Heidelberg, Berlin, Heidelberg, pp 87-114. doi:10.1007/978-3-642-38146-1_6

Westwood JH, Yoder JI, Timko MP, dePamphilis CW. 2010. The evolution of parasitism in plants. TRENDS in Plant Science 15 (4): 227-235. DOI:10.1016/j.tplants.2010.01.004

Yoder JI, Gunathilake P, Jamison-McClung D 2009 Hemiparasitic Plants: Exploiting Their Host’s Inherent Nature to Talk. In: Plant-Environment Interactions. pp 85-100. doi:10.1007/978-3-540-89230-4_5

Yoshida S, Cui S, Ichihashi Y, Shirasu K. 2016. The haustorium, a specialized invasive organ in parasitic plants. Annual Reviews in Plant Biology 67: 643-667. DOI:10.1146/annurev-arplant-043015-111702

How to Cite
Montes-Hernández, E., Sandoval-Zapotitla, E., Bermúdez-Torres, K., Trejo-Espino, J. L., & Trejo-Tapia, G. (2019). Hemiparasitic interaction between Castilleja tenuiflora (Orobanchaceae) and Baccharis conferta (Asteraceae): haustorium anatomy and C- and N-fluxes. Botanical Sciences, 97(2), 192-201. https://doi.org/10.17129/botsci.2100