Why do mixotrophic plants stay green? A comparison between green and achlorophyllous orchid individuals in situ

Ecological Monographs

Volumn 83, Issue 1, 2013, Pages 95-117

  Roy, M ^a   Gonneau, C ^a   Rocheteau, A ^a,b   Berveiller, D ^c,d   Thomas, J C ^e   Damesin, C ^c,d   Selosse, M A ^a  

^a CNRS   (France)

^b CENTRE D ECOLOGIE FONCTIONNELLE ET EVOLUTIVE   (France)

^c UNIVERSITÉ PARIS SUD   (France)

^d UNIVERSITÉ PARIS SACLAY   (France)

^e ECOLE NORMALE SUPÉRIEURE   (France)

Author keywords

Autotrophy; Dormancy; Fruit set; Herbivory; Mycorrhizae; Neottieae; Orchids; Parasitic load; Partial mycoheterotrophy; Plant phenology; Seed germination

Indexed keywords

ADAPTATION; ALGA; COMPARATIVE STUDY; EMERGENCE; EVOLUTIONARY BIOLOGY; FUNGUS; HERBIVORE; METABOLISM; OPTIMIZATION; ORCHARD; PHOTOSYNTHESIS; PLANT COMMUNITY; SPECIES DIVERSITY;

ALGAE; CEPHALANTHERA DAMASONIUM; FUNGI; NEOTTIEAE; ORCHIDACEAE;

EID: 84877121680     PISSN: 00129615     EISSN: 15577015     Source Type: Journal    
DOI: 10.1890/11-2120.1     Document Type: Article

References (107)

1. Abadie, J. C., U. Puttsepp, G. Gebauer, A. Faccio, P. Bonfante, and M.-A. Selosse. 2006. Cephalanthera longifolia (Neottieae, Orchidaceae) is mixotrophic: a comparative study between green and nonphotosynthetic individuals. Canadian Journal of Botany 84: 1462-1477.
2. Amthor, J. S. 1994. Higher plant respiration and its relationships to photosynthesis. Pages 71-101 in E. D. Schulze and M. M. Caldwell, editors. Ecophysiology of photosynthesis (Ecological Studies Volume 100). Springer-Verlag, Berlin, Germany.
3. Barkan, A. 2011. Expression of plastid genes: organelle-specific elaborations on a prokaryotic scaffold. Plant Physiology 155: 1520-1532.
4. Bell, T. L., M. A. Adams, and H. Rennenberg. 2011. Attack on all fronts: functional relationships between aerial and root parasitic plants and their woody hosts and consequences for ecosystems. Tree Physiology 31: 3-15.
5. Bidartondo, M. I., B. Burghardt, G. Gebauer, T. D. Bruns, and D. J. Read. 2004. Changing partners in the dark: isotopic and molecular evidence of ectomycorrhizal liaisons between forest orchids and trees. Proceedings of the Royal Society of London B 271: 1799-1806.
6. Björkman, E. 1960. Monotropa hypopitys L. and epiparasite on tree roots. Physiologia Plantarum 13: 308-327.
7. Bjorkman, O. 1981. Response to different quantum flux. Pages 57-107 in O. L. Lange, P. S. Nobal, L. B. Osmond, and H. Ziegler, editors. Physiological plant ecology. I. Response to the physical environment. Springer-Verlag, Berlin, Germany.
8. Bjorkman, O., and B. Demmin-Adams. 1995. Regulation of photosynthesis light energy capture, conversion, and dissipation in leaves of higher plants. Pages 17-47 in E.-D. Schulze and B. Caldwell, editors. Ecophysiology of photosynthesis. Springer-Verlag, New York, New York, USA.
9. Breshears, D. D., et al. 2005. Regional vegetation die-off in response to global-change-type drought. Proceedings of the National Academy of Sciences USA 102: 15144-15148.
10. Cameron, D. D., K. Preiss, G. Gebauer, and D. J. Read. 2009. The chlorophyll-containing orchid Corallorhiza trifida derives little carbon through photosynthesis. New Phytologist 183: 358-364.
11. Cernusak, L. A., D. J. Arthur, J. S. Pate, and G. D. Farquhar. 2003. Water relations link carbon and oxygen isotope discrimination to phloem sap sugar concentration in Eucalyptus globulus. Plant Physiology 131: 1544-1554.
12. 3 plants? Review and synthesis of current hypotheses. Functional Plant Biology 36: 199-213.
13. Claessens, J., and J. Kleynen. 2005. Pollination in the European orchids: four examples. Pages 572-577 in A. Raynal-Roques, A. Roguenant, and D. Prat, editors. Proceedings of the 18th world orchid conference. Naturalia Publications, Dijon, France.
14. Cleland, E. E., and W. S. Harpole. 2010. Nitrogen enrichment and plant communities. Annals of the New York Academy of Sciences 1195: 46-61.
15. Correll, D. S. 1950. Native orchids of North America north of Mexico. Chronica Botanica, Waltham, Massachusetts, USA.
16. Crane, K. W., and J. P. Grover. 2010. Coexistence of mixotrophs, autotrophs, and heterotrophs in planktonic microbial communities. Journal of Theoretical Biology 262: 517-527.
17. da Silva, M., and O. Liparini Pereira. 2011. Pseudocercospora epidendri sp. nov. on the neotropical orchid Epidendrum secundum from Brazil. Mycotaxon 118: 95-101.
18. Doring, T. F., and L. Chittka. 2007. Visual ecology of aphids: a critical review on the role of colours in host finding. Arthropod Plant Interactions 1: 3-16.
19. Everroad, C., C. Six, F. Partensky, J. C. Thomas, J. Holtzendorff, and A. M. Wood. 2006. Biochemical bases of type IV chromatic adaptation in marine Synechococcus spp. Journal of Bacteriology 188: 3345-3356.
20. Feldmann, K. A. 1991. T-DNA insertion mutagenesis in Arabidopsis: mutational spectrum. Plant Journal 1: 71-82.
21. Freudenstein, J. V., and C. F. Barrett. 2010. Mycoheterotrophy and diversity in Orchidaceae. Pages 25-37 in O. Seberg, G. Peterson, A. Barfod, and J. I. Davis, editors. Diversity, phylogeny, and evolution in the monocotyledons. Aarhus University Press, Aarhus, Denmark.
22. Gange, A. C., and H. M. West. 1994. Interactions between arbuscular mycorrhizal fungi and foliar-feeding Insects in Plantago lanceolata L. New Phytologist 128: 79-87.
23. 15N natural abundance of autotrophic and mycoheterotrophic orchids provides insight into nitrogen and carbon gain from fungal association. New Phytologist 160: 209-223.
24. Girlanda, M., M.-A. Selosse, D. Cafasso, F. Brilli, S. Delfine, R. Fabbian, S. Ghignone, P. Pinelli, R. Segreto, F. Loreto, S. Cozzolino, and S. Perotto. 2006. Inefficient photosynthesis in the Mediterranean orchid Limodorum abortivum is mirrored by specific association to ectomycorrhizal Russulaceae. Molecular Ecology 15: 491-504.
25. Gockel, G., and W. Hachtel. 2000. Complete gene map of the plastid genome of the nonphotosynthetic euglenoid flagellate Astasia longa. Protist 15: 347-351.
26. Hannaert, V., E. Saavedra, F. Duffieux, J. P. Szikora, D. J. Rigden, P. A. Michels, and F. R. Opperdoes. 2003. Plant-like traits associated with metabolism of Trypanosoma parasites. Proceedings of National Academy of Sciences USA 100: 1067-1071.
27. Heizmann, P., J. Doly, Y. Hussein, P. Nicolas, V. Nigon, and G. Bernardi. 1981. The chloroplast genome of bleached mutants of Euglena gracilis. Biochimica et Biophysica Acta 653: 412-415.
28. Jacquemyn, H., R. Brys, and E. Jongejans. 2010. Seed limitation restricts population growth in shaded populations of a perennial woodland orchid. Ecology 91: 119-129.
29. Julou, T., B. Burghardt, G. Gebauer, D. Berveiller, C. Damesin, and M.-A. Selosse. 2005. Mixotrophy in orchids: insights from a comparative study of green individuals and nonphotosynthetic individuals of Cephalanthera damasonium. New Phytologist 166: 639-653.
30. Keeling, P. J. 2010. The endosymbiotic origin, diversification and fate of plastids. Philosophical Transactions of the Royal Society B 365: 729-748.
31. Keitel, C., M. A. Adams, T. Holst, A. Matzarakis, H. Mayer, H. Rennenberg, and A. Gessler. 2003. Carbon and oxygen isotope composition of organic compounds in the phloem sap
32. provides a short-term measure for stomatal conductance of European beech (Fagus sylvatica L.). Plant, Cell and Environment 26: 1157-1168.
33. Kempel, A., R. Brandl, and M. Schädler. 2009. Symbiotic soil microorganisms as players in aboveground plant herbivore interactions the role of rhizobia. Oikos 118: 634-640.
34. Kiers, E. T., et al. 2011. Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333: 880-882.
35. Klimesnova, J. 2007. Root-sprouting in myco-heterotrophic plants: prepackaged symbioses or overcoming meristem limitation? New Phytologist 173: 8-10.
36. Klooster, M. R., D. L. Clark, and T. M. Culle. 2009. Cryptic bracts facilitate herbivore avoidance in the mycoheterotrophic plant Monotropsis odorata (Ericaceae). American Journal of Botany 96: 1-9.
37. Krause, K. 2008. From chloroplasts to "cryptic" plastids: evolution of plastid genomes in parasitic plants. Current Genetics 54: 111-121.
38. Látr, A. M. Čuříková, M. Baláž, and J. Jurčák. 2008. Mycorrhizas of Cephalanthera longifolia and Dactylorhiza majalis, two terrestrial orchids. Annales Botanici Fennici 45: 281-289.
39. Lawson, T. 2009. Guard cell photosynthesis and stomatal function. New Phytologist 181: 13-34.
40. Leake, J. R. 1994. The biology of myco-heterotrophic (saprophytic) plants. New Phytologist 127: 171-216.
41. Leake, J. R. 2004. Myco-heterotroph/epiparasitic plant interactions with ectomycorrhizal and arbuscular mycorrhizal fungi. Current Opinion in Plant Biology 7: 422-428.
42. Leake, J. R., and D. D. Cameron. 2010. Physiological ecology of mycoheterotrophy. New Phytologist 185: 601-605.
43. Lim, L., and G I. McFadden. 2010. The evolution, metabolism and functions of the apicoplast. Philosophical Transactions of the Royal Society B 365: 749-763.
44. Lopez, S., F. Rousset, F. H. Shaw, R. G Shaw, and O. Ronce. 2008. Migration load in plants: role of pollen and seed dispersal in heterogeneous landscapes. Journal of Evolutionary Biology 21: 294-309.
45. Mairold, F., and F. Weber. 1950. Notiz über Cephalanthera albinos. Protoplasma 39: 275-277.
46. Martos, F., M. Dulormne, T. Pailler, P. Bonfante, A. Faccio, J. Fournel, M.-P. Dubois, and M.-A. Selosse. 2009. Independent recruitment of saprotrophic fungi as mycorrhizal partners by tropical achlorophyllous orchids. New Phytologist 184: 668-681.
47. Matsuda, Y., A. Amiya, and S. I. Ito. 2009. Colonization patterns of mycorrhizal fungi associated with two rare orchids, Cephalanthea falcata and C. erecta. Ecological Research 24: 1023-1031.
48. Matsuda, Y., S. Shimizu, M. Mori, Ito S.-I., and M.-A. Selosse. 2012. Seasonal and environmental changes of mycorrhizal associations and heterotrophy levels in mixotrophic Pyrola japonica growing under different light environments. American Journal of Botany 99: 1177-1188.
49. McDowell, N, W. T. Pockman, C. D. Allen, D. D. Breshears, N. Cobb, T. Kolb, J. Plaut, J. Sperry, A. West, D. G Williams, and E. A. Yepez. 2008. Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytologist 178: 719-739.
50. Merlot, S., A. C. Mustilli, B. Genty, H. North, V. Lefebvre, B. Sotta, A. Vavasseur, and J. Giraudat. 2002. Use of infrared thermal imaging to isolate Arabidopsis mutants defective in stomatal regulation. Plant Journal 30: 601-609.
51. Micheneau, C, K. J. Duffy, R. J. Smith, L. J. Stevens, J. C. Stout, L. Civeyrel, R. S. Cowan, and M. F. Fay. 2010. Plastid microsatellites for the study of genetic variability in the widespread Cephalanthera longifolia, C. damasonium and C rubra (Neottieae, Orchidaceae), and cross-amplification in other Cephalanthera species. Botanical Journal of the Linnean Society B 163: 181-193.
52. Motomura, H., M.-A. Selosse, F. Martos, A. Kagawa, and T. Yukawa. 2010. Mycoheterotrophy evolved from mixotrophic ancestors: evidence in Cymbidium (Orchidaceae). Annals of Botany 106: 573-581.
53. Okamoto, N., and I. Inouye. 2005. A secondary symbiosis in progress? Science 310: 287.
54. Ortiz-Barney, E., and J. D. Ackerman. 1999. The cost of selfing in Encyclia cochleata (Orchidaceae). Plant Systematics and Evolution 219: 55-64.
55. Oxford, G. S., and R. G. Gillespie. 1998. Evolution and ecology of spider coloration. Annual Review of Entomology 43: 619-643.
56. Pedersen, H. Æ., S. Watthana, M. Roy, S. Suddee, and M.-A. Selosse. 2009. Cephalanthera exigua rediscovered: new insights in the taxonomy, habitat requirements and breeding system of a rare mycoheterotrophic orchid. Nordic Journal of Botany 27: 460-468.
57. Preiss, K., I. K. U. Adam, and G. Gebauer. 2010. Irradiance governs exploitation of fungi: fine-tuning of carbon gain by two partially myco-heterotrophic orchids. Proceedings of the Royal Society B 277: 1333-1336.
58. Press, M. C., S. Smith, and G. R. Stewart. 1991. Carbon acquisition and assimilation in parasitic plants. Functional Ecology 5: 278-283.
59. Primack, R., and E. Stacy. 1998. Cost of reproduction in the pink lady's slipper orchid (Cypripedium acaule, Orchidaceae): an eleven-year experimental study of three populations. American Journal of Botany 85: 1672-1679.
60. R Development Core Team. 2010. R: a language and environment for statistical computing. Version 2.10.1. R Foundation for Statistical Computing, Vienna, Austria. http://cran.r-project.org/bin/windows/base/old/2.10.1/
61. Rasmussen, H. N. 1995. Terrestrial orchids: from seed to mycotrophic plant. Cambridge University Press, Cambridge, UK.
62. Rasmussen, H. N., and D. F. Whigham. 2002. Phenology of roots and mycorrhiza in five orchid species differing in phototrophic strategy. New Phytologist 154: 797-807.
63. Renner, O. 1938. Uber blasse, saprophytische Cephalanthera alba und Epipactis latifolia. Flora 132: 225-233.
64. Reyes-Prieto, A., A. Moustafa, and D. Bhattacharya. 2008. Multiple genes of apparent algal origin suggest ciliates may once have been photosynthetic. Current Biology 18: 956-962.
65. 2 and abscissic acid. Plant, Cell and Environment 29: 1595-1605.
66. Rosati, G., L. Barsanti, V. Passarelli, A. Giambelluca, and P. Gualtieri. 1996. Ultrastructure of a novel nonphotosynthetic Euglena mutant. Micron 27: 367-373.
67. Roy, M., S. Watthana, A. Stier, F. Richard, S. Vessabutr, and M.-A. Selosse. 2009a. Two mycoheterotrophic orchids from Thailand tropical dipterocarpacean forest associate with a broad diversity of ectomycorrhizal fungi. BMC Biology 7: 51.
68. Roy, M., T. Yagame, M. Yamato, K. Iwase, C. Heinz, A. Faccio, P. Bonfante, and M.-A. Selosse. 2009b. Ectomycorrhizal Inocybe species associate with the mycoheterotrophic orchid Epipogium aphyllum but not with its asexual propagules. Annals of Botany 104: 595-610.
69. Salmia, A. 1986. Chlorophyll-free form of Epipactis helleborine (Orchidaceae) in SE Finland. Annals of Botany Fennici 23: 49-57.
70. Salmia, A. 1988. Endomycorrhizal fungus in chlorophyll-free and green forms of the terrestrial orchid Epipactis helleborine. Karstenia 28: 3-18.
71. Salmia, A. 1989a. Features of endomycorrhizal infection of chlorophyll-free and green forms of Epipactis helleborine (Orchidaceae). Annals of Botany Fennici 26: 15-26.
72. Salmia, A. 1989b. General morphorlogy and anatomy of chlorophyll-free and green forms of Epipactis helleborine (Orhcidaceae). Annals of Botany Fennici 26: 95-105.
73. Scacchi, R., G. De Angelis, and R. M. Corbo. 1991. Effect of the breeding system on the genetic structure in three Cephalanthera spp. (Orchidaceae). Plant Systematics and Evolution 176: 53-61.
74. Scappaticci, C., and G. Scappaticci. 1998. Epipactis microphylla (Ehrhardt) Swartz lusus rosea. Pages 68-70 in G. Scappaticci, editor. Cahiers de la Societé Francaise d'Orchidophilie, leres journées Rencontres Orchidophiles Rhǒnes-Alpes. Societe Française d'Orchidophilie, Paris, France.
75. Schoonhoven, L. M., J. J. A. van Loon, and M. Dicke. 2005. Insect-plant biology. Second edition. Oxford University Press, Oxford, UK.
76. Selosse, M.-A., A. Faccio, G. Scappaticci, and P. Bonfante. 2004. Chlorophyllous and achlorophyllous specimens of Epipactis microphylla (Neottieae, Orchidaceae) are associated with ectomycorrhizal septomycetes, including truffles. Microbial Ecology 47: 416-426.
77. Selosse, M.-A., and F. Le Tacon. 1998. The land flora: a phototroph-fungus partnership? Trends in Ecology and Evolution 13: 15-20.
78. Selosse, M.-A., F. Richard, X. H. He, and S. W. Simard. 2006. Mycorrhizal networks: des liaisons dangereuses? Trends in Ecology and Evolution 21: 621-628.
79. Selosse, M.-A., and F. Rousset. 2011. The plant-fungal marketplace. Science 333: 828-829.
80. Selosse, M.-A., and M. Roy. 2009. Green plants that feed on fungi: facts and questions about mixotrophy. Trends in Plant Sciences 14: 64-70.
81. Selosse, M.-A., M. Weiss, J. L. Jany, and A. Tillier. 2002. Communities and populations of sebacinoid basidiomycetes associated with the achlorophyllous orchid Neottia nidus-avis (L.) LCM Rich. and neighbouring tree ectomycorrhizae. Molecular Ecology 11: 1831-1844.
82. Shefferson, R. P. 2009. The evolutionary ecology of vegetative dormancy in mature herbaceous perennial plants. Journal of Ecology 97: 1000-1009.
83. Shefferson, R. P., T. Kull, and K. Tali. 2005. Adult whole-plant dormancy induced by stress in long-lived orchids. Ecology 86: 3099-3104.
84. Shefferson, R. P., T. Kull, and K. Tali. 2006. Demographic response to shading and defoliation in two woodland orchids. Folia Geobotanica 41: 95-106.
85. Shefferson, R. P., M. K. McCormick, D. F. Whigham, and J. P. O'Neill. 2011. Life history strategy in herbaceous perennials: inferring demographic patterns from the aboveground dynamics of a primarily subterranean, myco-heterotrophic orchid. Oikos 120: 1291-1300.
86. Shefferson, R. P., J. Proper, S. R. Beissinger, and E. L. Simms. 2003. Life history trade-offs in a rare orchid: the costs of flowering, dormancy, and sprouting. Ecology 84: 1199-1206.
87. Shefferson, R. P., and K. Tali. 2007. Dormancy is associated with decreased adult survival in the burnt orchid, Neotinea ustulata. Journal of Ecology 95: 217-225.
88. Shimazaki, K. I., M. Doi, S. M. Assmann, and T. Kinoshita. 2007. Light regulation of stomatal movement. Annual Review of Plant Biology 58: 219-247.
89. Simard, S. W., and D. M. Durall. 2004. Mycorrhizal networks: a review of their extent, function, and importance. Canadian Journal of Botany 82: 1140-1165.
90. Sletvold, N., and J. Ågren. 2011. Among-population variation in costs of reproduction in the long-lived orchid Gymnadenia conopsea: an experimental study. Oecologia 167: 461-468.
91. Smedley, M. P., T. E. Dawson, J. P. Comstock, L. A. Donovan, D. E. Sherrill, C. S. Cook, and J. R. Ehleringer. 1991. Seasonal carbon isotope discrimination in a grassland community. Oecologia 85: 314-320.
92. Stearns, S. C. 1992. The evolution of life histories. Oxford University Press, Oxford, UK.
93. Stockel, M., C. Meyer, and G. Gebauer. 2011. The degree of mycoheterotrophic carbon gain in green, variegated and vegetative albino individuals of Cephalanthera damasonium is related to leaf chlorophyll concentrations. New Phytologist 189: 790-796.
94. Talbott, L. D., J. X. Zhu, S. W. Han, and E. Zeiger. 2002. Phytochrome and blue light-mediated stomatal opening in the orchid Paphiopedilum. Plant and Cell Physiology 43: 639-646.
95. Tatarenko, I. V. 2002. Intensity of mycorrhizal infection in some orchid populations in Japan. Pages 167-183 in P. Kindlmann, J. H. Willems, and D. F. Whigham, editors. Trends and fluctuations and underlying mechanisms in terrestrial orchid populations. Backhuys, Leiden, The Netherlands.
96. Taylor, D. L., and T. D. Bruns. 1997. Independent, specialized invasions of ectomycorrhizal mutualism by two nonphoto-synthetic orchids. Proceedings of the National Academy of Sciences USA 94: 4510-4515.
97. Tedersoo, L., P. Pellet, U. Koljalg, and M.-A. Selosse. 2007. Parallel evolutionary paths to mycoheterotrophy in under-storey Ericaceae and Orchidaceae: ecological evidence for mixotrophy in Pyroleae. Oecologia 151: 206-217.
98. Těšitel, J., L. Plavcová, and D. D. Cameron. 2010. Interactions between hemiparasitic plants and their hosts. The importance of organic carbon transfer. Plant Signaling and Behavior 5: 1072-1076.
99. Tranchida-Lombardo, V., M. Roy, E. Bugot, G. Santoro, U. Puttsep, M.-A. Selosse, and S. Cozzolino. 2010. Spatial repartition and genetic relationship of green and non-photosynthetic individuals in mixed populations of Cephalanthera orchids. Plant Biology 12: 659-667.
100. Trudell, S. A., P. T. Rygiewicz, and R. L. Edmonds. 2003. Nitrogen and carbon stable isotope abundances support the myco-heterotrophic nature and host-specificity of certain achlorophyllous plants. New Phytologist 160: 391-401.
101. Van den Kinderen, G. 1995. A method for the study of field germinated seeds of terrestrial orchids. Lindleyana 10: 68-73.
102. Westwood, J. H., J. I. Yoder, M. Timko, and C. W. de Pamphilis. 2010. The evolution of parasitism in plants. Trends in Plant Science 15: 227-235.
103. Williams, J. H. H., and J. F. Farrar. 1990. Control of barley root respiration. Physiologia Plantarum 79: 259-266.
104. Yagame, T., T. Orihara, M.-A. Selosse, M. Yamato, and K. Iwase. 2012. Mixotrophy of Platanthera minor, an orchid associated with ectomycorrhiza- forming Ceratobasidiaceae fungi. New Phytologist 193: 178-197.
105. Yukawa, T., and W. L. Stern. 2002. Comparative vegetative anatomy and systematics of Cymbidium (Cymbidieae: Or-chidaceae). Botanical Journal of the Linnean Society 138: 383-419.
106. Zhang, S. B., H. Hu, and Z. R. Li. 2010. Variation of photosynthetic capacity with leaf age in an alpine orchid, Cypripedium flavum. Acta Physiologiae Plantarum 30: 381-388.
107. Zimmer, K., N. A. Hynson, G. Gebauer, E. B. Allen, M. F. Allen, and D. J. Read. 2007. Wide geographical and ecological distribution of nitrogen and carbon gains from fungi in Pyroloids and Monotropoids (Ericaceae) and in orchids. New Phytologist 175: 166-175.