Root-hemiparasitic plants of the genus Rhinanthus acquire resources through a water-wasting physiological strategy based on high transpiration rate mediated by the accumulation of osmotically active compounds and constantly open stomata. Interestingly, they were also documented to withstand moderate water stress which agrees with their common occurrence in rather dry habitats. Here, we focused on the water-stress physiology of Rhinanthus alectorolophus by examining gas exchange, water relations, stomatal density, and biomass production and its stable isotope composition in adult plants grown on wheat under contrasting (optimal and drought-inducing) water treatments. We also tested the effect of water stress on the survival of Rhinanthus seedlings, which were watered either once (after wheat sowing), twice (after wheat sowing and the hemiparasite planting) or continuously (twice and every sixth day after that). Water shortage significantly reduced seedling survival as well as the biomass production and gas exchange of adult hemiparasites. In spite of that drought-stressed and even wilted plants from both treatments still considerably photosynthesized and transpired. Strikingly, low-irrigated plants exhibited significantly elevated photosynthetic rate compared with high-irrigated plants of the same water status. This might relate to biochemical adjustments of these plants enhancing the resource uptake from the host. Moreover, low-irrigated plants did not acclimatize to water stress by lowering their osmotic potential, perhaps due to the capability to tolerate drought without such an adjustment, as their osmotic potential at full turgor was already low. Contrary to results of previous studies, hemiparasites seem to close their stomata in response to severe drought stress and this happens probably passively after turgor is lost in guard cells. The physiological traits of hemiparasites, namely the low osmotic potential associated with their parasitic lifestyle and the ability to withstand drought and recover from the wilting likely enable them to grow in dry habitats. However, the absence of osmotic adjustment of adults and sensitivity of seedlings to severe drought stress demonstrated here may result in a substantial decline of the hemiparasitic species with ongoing climate change.

Department of Botany and Zoology Masaryk University Brno Czech Republic

Faculty of Science University of South Bohemia České Budějovice Czech Republic

Institute of Botany of the Czech Academy of Sciences Třeboň Czech Republic

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Lambers H, Chapin F III, Pons T, editors. Plant Physiological Ecology. 2nd ed New York: Springer-Verlag; 2008. 10.1016/j.aos.2008.04.001 DOI

Sun WQ. Methods for the study of water relations under desiccation stress In: Black M, Pritchard HW, editors. Desiccation and survival in plants: Drying without dying. Wallingford: CABI Publishing; 2002. pp. 47–91. 10.1079/9780851995342.0000 DOI

Westwood JH. The physiology of the established parasite–host association In: Joel D, Gressel J, Musselman LJ, editors. Parasitic Orobanchaceae: Parasitic mechanisms and control strategies. Berlin: Springer-Verlag; 2013. pp. 87–114. 10.1007/978-3-642-38146-1 DOI

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

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

Těšitel J, Těšitelová T, Fisher JP, Lepš J, Cameron DD. Integrating ecology and physiology of root-hemiparasitic interaction: interactive effects of abiotic resources shape the interplay between parasitism and autotrophy. New Phytol. 2014;205: 350–360. 10.1111/nph.13006 PubMed DOI

Selosse M-A, Charpin M, Not F. Mixotrophy everywhere on land and in water: the grand écart hypothesis. Ecol Lett. 2017;20: 246–263. 10.1111/ele.12714 PubMed DOI

Dörr I. How Striga parasitizes its host: a TEM and SEM study. Ann Bot. 1997;79: 463–472. 10.1006/anbo.1996.0385 DOI

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

Press MC, Graves JD, Stewart GR. Transpiration and carbon acquisition in root hemiparasitic angiosperms. J Exp Bot. 1988;39: 1009–1014. 10.1093/jxb/39.8.1009 DOI

Stewart GRG, Press MCM. The physiology and biochemistry of parasitic angiosperms. Annu Rev Plant Physiol Mol Biol. 1990;41: 127–151. 10.1146/annurev.pp.41.060190.001015 DOI

Jiang F, Jeschke WD, Hartung W. Water flows in the parasitic association Rhinanthus minor/Hordeum vulgare. J Exp Bot. 2003;54: 1985–1993. 10.1093/jxb/erg212 PubMed DOI

Ehleringer JR, Marshall JD. Water relations In: Press MC, Graves JD, editors. Parasitic plants. London: Chapman & Hall; 1995. pp. 125–140.

Jiang F, Jeschke WD, Hartung W. Contents and flows of assimilates (mannitol and sucrose) in the hemiparasitic Rhinanthus minor/Hordeum vulgare association. Folia Geobot. 2005;40: 195–203. 10.1007/BF02803234 DOI

Smith S, Stewart GR. Effect of potassium levels on the stomatal behavior of the hemi-parasite Striga hermonthica. Plant Physiol. 1990;94: 1472–1476. 10.1104/pp.94.3.1472 PubMed DOI PMC

Govier RN, Brown JGS, Pate JS. Hemiparasitic nutrition in angiosperms. II. Root haustoria and leaf glands of Odontites verna (Bell.) Dum. and their relevance to the abstraction of solutes from the host. New Phytol. 1968;67: 963–972. 10.1111/j.1469-8137.1968.tb06407.x DOI

Těšitel J, Tesařová M. Ultrastructure of hydathode trichomes of hemiparasitic Rhinanthus alectorolophus and Odontites vernus: how important is their role in physiology and evolution of parasitism in Orobanchaceae? Plant Biol. 2013;15: 119–125. 10.1111/j.1438-8677.2012.00610.x PubMed DOI

Světlíková P, Hájek T, Těšitel J. Hydathode trichomes actively secreting water from leaves play a key role in the physiology and evolution of root-parasitic rhinanthoid Orobanchaceae. Ann Bot. 2015;116: 61–68. 10.1093/aob/mcv065 PubMed DOI PMC

Meusel H, Jäger E, Rauschert S, Weinert E. Vergleichende Chorologie der zentraleuropäischen Flora. Jena: Gustav Fischer Verlag; 1978.

Hejcman M, Schellberg J, Pavlů V. Competitive ability of Rhinanthus minor L. in relation to productivity in the Rengen grassland experiment. Plant, Soil Environ. 2011;57: 45–51.

Těšitel J, Mládek J, Horník J, Těšitelová T, Adamec V, Tichý L. Suppressing competitive dominants and community restoration with native parasitic plants using the hemiparasitic Rhinanthus alectorolophus and the dominant grass Calamagrostis epigejos. J Appl Ecol. 2017;54; 1487–1495. 10.1111/1365-2664.12889 DOI

Těšitel J, Fibich P, de Bello F, Chytrý M, Lepš J. Habitats and ecological niches of root-hemiparasitic plants: an assessment based on a large database of vegetation plots. Preslia. 2015;87: 87–108.

Ducarme V, Wesselingh R. Performance of two Rhinanthus species under different hydric conditions. Plant Ecol. 2009;206: 263–277. 10.1007/s11258-009-9640-1 DOI

Jiang F, Jeschke WD, Hartung W. Abscisic acid (ABA) flows from Hordeum vulgare to the hemiparasite Rhinanthus minor and the influence of infection on host and parasite abscisic acid relations. J Exp Bot. 2004;55: 2323–2329. 10.1093/jxb/erh240 PubMed DOI

Těšitel J, Říha P, Svobodová Š, Malinová T, Štech M. Phylogeny, life history evolution and biogeography of the Rhinanthoid Orobanchaceae. Folia Geobot. 2010;45: 347–367. 10.1007/s12224-010-9089-y DOI

McNeal JR, Bennett JR, Wolfe AD, Mathews S. Phylogeny and origins of holoparasitism in Orobanchaceae. Am J Bot. 2013;100: 971–983. 10.3732/ajb.1200448 PubMed DOI

Zopfi H. Ecotypic variation in Rhinanthus alectorolophus (Scopoli) Pollich (Scrophulariaceae) in relation to grassland management. II: The genotypic basis of seasonal ecotypes. Flora. Elsevier Masson SAS; 1993;188: 153–173. 10.1016/S0367-2530(17)32261-2 DOI

Skála Z, Štech M. Rhinanthus L In: Slavík B, editor. Květena České Republiky [Flora of the Czech Republic] 6 Praha: Academia; 2000. pp. 462–471.

Blažek P, Lepš J. Victims of agricultural intensification: MOWING date affects Rhinanthus spp. regeneration and fruit ripening. Agric Ecosyst Environ. 2015;211: 10–16. 10.1016/j.agee.2015.04.022 DOI

Klaren CH, Janssen G. Physiological changes in the hemiparasite Rhinanthus serotinus before and after attachment. Physiol Plant. 1978;42: 151–155. 10.1111/j.1399-3054.1978.tb01556.x DOI

Chaves MM, Maroco JP, Pereira JS. Understanding plant responses to drought—from genes to the whole plant. Funct Plant Biol. 2003;30: 239–264. 10.1071/FP02076 PubMed DOI

Turner NC. Techniques and experimental approaches for the measurement of plant water status. Plant Soil. 1981;58: 339–366. 10.1007/BF02180062 DOI

Koide RT, Robichaux RH, Morse SR, S C.M. Plant water status, hydraulic resistance and capacitance In: Pearcy RW, Ehleringer J, Mooney HA, Rundel PW, editors. Plant physiological ecology: Field methods and instrumentation. London: Chapman & Hall; 1989. pp. 161–183. 10.1016/0169-5347(90)90241-5 DOI

Tyree MT, Hammel HT. The measurement of the turgor pressure and the water relations of plants by the pressure-bomb technique. J Exp Bot. 1972;23: 267–282. 10.1093/jxb/23.1.267 DOI

Crawley M. The R Book. Chichester: John Wiley and Sons; 2007. 10.1198/016214502760047131 DOI

Harrington DP, Fleming TR. A class of rank test procedures for censored survival data. Biometrika. 1982;69: 553–566. 10.1093/biomet/69.3.553 DOI

R Core Team. R: a language and environment for statistical computing [Internet]. Vienna, Austria: R Foundation for Statistical Computing; 2013. Available: http://www.r-project.org/

Van Hulst R, Shipley B, Theriault A. Why is Rhinanthus minor (Scrophulariaceae) such a good invader? Can J Bot. 1987;65: 2373–2379. 10.1139/b87-322 DOI

Ameloot E, Verheyen K, Bakker JP, Vries Y De, Hermy M. Long-term dynamics of the hemiparasite Rhinanthus angustifolius and its relationship with vegetation structure. J Veg Sci. 2006;17: 637–646. 10.1111/j.1654-1103.2006.tb02487.x DOI

Inoue T, Yamauchi Y, Eltayeb AH, Samejima H, Babiker AGT, Sugimoto Y. Gas exchange of root hemi-parasite Striga hermonthica and its host Sorghum bicolor under short-term soil water stress. Biol Plant. 2013;57: 773–777. 10.1007/s10535-013-0348-7 DOI

Ullmann I, Lange OL, Ziegler H, Ehleringer J, Schulze ED, Cowan IR. Diurnal courses of leaf conductance and transpiration of mistletoes and their hosts in Central Australia. Oecologia. 1985;67: 577–587. 10.1007/BF00790030 PubMed DOI

Flexas J, Bota J, Galmes J, Medrano H, Ribas-Carbo M. Keeping a positive carbon balance under adverse conditions: responses of photosynthesis and respiration to water stress. Physiol Plant. 2006;127: 343–352. 10.1111/j.1399-3054.2005.00621.x DOI

Grassi G, Magnani F. Stomatal, mesophyll conductance and biochemical limitations to photosynthesis as affected by drought and leaf ontogeny in ash and oak trees. Plant, Cell Environ. 2005;28: 834–849. 10.1111/j.1365-3040.2005.01333.x DOI

Yan W, Zhong Y, Shangguan Z. A meta-analysis of leaf gas exchange and water status responses to drought. Sci Rep. 2016;6: 20917 10.1038/srep20917 PubMed DOI PMC

Flexas J, Medrano H. Drought-inhibition of photosynthesis in C3 plants: Stomatal and non-stomatal limitations revisited. Ann Bot. 2002;89: 183–189. 10.1093/aob/mcf027 PubMed DOI PMC

Kubiske ME, Abrams MD. Ecophysiological analysis of woody species in contrasting temperate communities during wet and dry years. Oecologia. 1994;98: 303–312. 10.1007/BF00324218 PubMed DOI

Goldstein G, Rada F, Sternberg L, Burguera J, Burguera M, Orozco A, et al. Gas exchange and water balance of a mistletoe species and its mangrove hosts. Oecologia. 1989;78: 176–183. 10.1007/BF00377153 PubMed DOI

Lenz TI, Wright IJ, Westoby M. Interrelations among pressure-volume curve traits across species and water availability gradients. Physiol Plant. 2006;127: 423–433. 10.1111/j.1399-3054.2006.00680.x DOI

Maury P, Mojayad F, Berger M, Planchon C. Photochemical response to drought acclimation in two sunflower genotypes. Physiol Plant. 1996;98: 57–66. 10.1111/j.1399-3054.1996.tb00675.x DOI

Krasser D, Kalapos T. Leaf water relations for 23 angiosperm species from steppe grasslands in Hungary. Community Ecol. 2000;1: 123–131. 10.1556/ComEc.1.2000.2.1 DOI

Fleta-Soriano E, Munné-Bosch S. Stress memory and the inevitable effects of drought: a physiological perspective. Front Plant Sci. 2016;7: 1–6. 10.3389/fpls.2016.00001 PubMed DOI PMC

Bruce TJA, Matthes MC, Napier JA, Pickett JA. Stressful “memories” of plants: evidence and possible mechanisms. Plant Sci. 2007;173: 603–608. 10.1016/j.plantsci.2007.09.002 DOI

Menezes-Silva PE, Sanglard LMP V., Ávila RT, Morais LE, Martins SC V., Nobres P, et al. Photosynthetic and metabolic acclimation to repeated drought events play key roles in drought tolerance in coffee. J Exp Bot. 2017;68: 4309–4322. 10.1093/jxb/erx211 PubMed DOI

Seel WE, Cooper RE, Press MC. Growth, gas exchange and water use efficiency of the facultative hemiparasite Rhinanthus minor associated with hosts differing in foliar nitrogen concentration. Physiol Plant. 1993;89: 64–70. 10.1111/j.1399-3054.1993.tb01787.x DOI

Cernusak LA, Pate JS, Farquhar GD. Oxygen and carbon isotope composition of parasitic plants and their hosts in southwestern Australia. Oecologia. 2004;139: 199–213. 10.1007/s00442-004-1506-6 PubMed DOI

Press MC, Shah N, Tuohy JM, Stewart GR. Carbon isotope ratios demonstrate carbon flux from C4 host to C3 parasite. Plant Physiol. 1987;85: 1143–1145. 10.1104/pp.85.4.1143 PubMed DOI PMC

Pate JS, Davidson NJ, Kuo J, Milburn JA. Water relations of the root hemiparasite Olax phyllanthi (Labill) R.Br. (Olacaceae) and its multiple hosts. Oecologia. 1990;84: 186–193. 10.1007/BF00318270 PubMed DOI

McAdam SAM, Brodribb TJ. Ancestral stomatal control results in a canalization of fern and lycophyte adaptation to drought. New Phytol. 2013;198: 429–441. 10.1111/nph.12190 PubMed DOI

Tombesi S, Nardini A, Frioni T, Soccolini M, Zadra C, Farinelli D, et al. Stomatal closure is induced by hydraulic signals and maintained by ABA in drought-stressed grapevine. Sci Rep. 2015;5: 12449 10.1038/srep12449 PubMed DOI PMC

Rodriguez-Dominguez CM, Buckley TN, Egea G, de Cires A, Hernandez-Santana V, Martorell S, et al. Most stomatal closure in woody species under moderate drought can be explained by stomatal responses to leaf turgor. Plant Cell Environ. 2016;39: 2014–2026. 10.1111/pce.12774 PubMed DOI

McAdam SAM, Brodribb TJ. Separating active and passive influences on stomatal control of transpiration. Plant Physiol. 2014;164: 1578–1586. 10.1104/pp.113.231944 PubMed DOI PMC

Phoenix GK, Press MC. Effects of climate change on parasitic plants: the root hemiparasitic Orobanchaceae. Folia Geobot. 2005;40: 205–216. 10.1007/BF02803235 DOI

Meehl GA, Stocker TF, Collins WD, Friedlingstein P, Gaye AT, Gregory JM, et al. Global Climate Projections In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt K, et al., editors. Climate Change 2007: The Physical Science Basis Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge, United Kingdom and New York, NY, USA: Cambridge University Press; 2007. pp. 747–846. 10.1080/07341510601092191 DOI