Abstract
Fungi show a high degree of morphological convergence. Regarded for a long time as an obstacle for phylogenetic studies, homoplasy has also been proposed as a source of information about underlying morphogenetic patterning mechanisms. The "local-activation and long-range inhibition principle" (LALIP), underlying the famous reaction–diffusion model proposed by Alan Turing in 1952, appears to be one of the universal phenomena that can explain the ontogenetic origin of seriate patterns in living organisms. Reproductive structures of fungi in the class Agaricomycetes show a highly periodic structure resulting in, for example, poroid, odontoid, lamellate or labyrinthic hymenophores. In this paper, we claim that self-organized patterns might underlie the basic ontogenetic processes of these structures. Simulations based on LALIP-driven models and covering a wide range of parameters show an absolute mutual correspondence with the morphospace explored by extant agaricomycetes. This could not only explain geometric particularities but could also account for the limited possibilities displayed by hymenial configurations, thus making homoplasy a direct consequence of the limited morphospace resulting from the proposed patterning dynamics.
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References
Agosti A, Antonietti PF, Ciarletta P, Grasselli M, Verani M (2017) A Cahn-Hilliard–type equation with application to tumor growth dynamics. Math Methods Appl Sci 40(18):7598–7626
Bailleul R, Manceau M, Touboul J (2020) A “numerical Evo-Devo” synthesis for the identification of pattern-forming factors. Cells 9(8):1840
Bard JB (1981) A model for generating aspects of zebra and other mammalian coat patterns. J Theor Biol 93(2):363–385
Benedix EH (1967) Bemerkenswerte Prolifikationen bei Blätterpilzen. Feddes Repertorium 74(3):201–207
Binder M, Larsson KH, Matheny PB, Hibbett DS (2010) Amylocorticiales ord. nov. and Jaapiales ord. nov.: early diverging clades of Agaricomycetidae dominated by corticioid forms. Mycologia 102(4):865–880
Birkebak JM, Mayor JR, Ryberg KM, Matheny PB (2013) A systematic, morphological and ecological overview of the Clavariaceae (Agaricales). Mycologia 105(4):896–911
Blagodatski A, Sergeev A, Kryuchkov M, Lopatina Y, Katanaev VL (2015) Diverse set of turing nanopatterns coat corneae across insect lineages. Proc Natl Acad Sci 112(34):10750–10755
Bloemendal S, Kück U (2013) Cell-to-cell communication in plants, animals, and fungi: a comparative review. Naturwissenschaften 100(1):3–19
Brinkmann F, Mercker M, Richter T, Marciniak-Czochra A (2018) Post-turing tissue pattern formation: advent of mechanochemistry. PLoS computational biology 14(7):e1006259
Bruns TD, Fogel R, White TJ, Palmer JD (1989) Accelerated evolution of a false-truffle from a mushroom ancestor. Nature 339(6220):140
Büscher TH, Kryuchkov M, Katanaev VL, Gorb SN (2018) Versatility of Turing patterns potentiates rapid evolution in tarsal attachment microstructures of stick and leaf insects (Phasmatodea). J R Soc Interface 15(143):20180281
Cahn JW, Hilliard JE (1958) Free energy of a nonuniform system I interfacial free energy. J Chem Phys 28(2):258–267
Cartwright JH (2002) Labyrinthine Turing pattern formation in the cerebral cortex. J Theor Biol 217(1):97–103
Chen CC, Cao B, Hattori T, Cui BK, Chen CY, Wu SH (2020) Phylogenetic placement of Paratrichaptum and reconsideration of gloeophyllales. Fungal Systemat Evol 5:119
Chen JJ, Cui BK, Dai YC (2016) Global diversity and molecular systematics of Wrightoporia s.l. (Russulales, Basidiomycota). Persoonia 37:21–36
Chiu SW, Moore D, Chang ST (1989) Basidiome polymorphism in Volvariella bombycina. Mycol Res 92(1):69–77
Chiu SW, Moore D, (1990) A mechanism for gill pattern formation in Coprinus cinereus. Mycol Res 94(3):320–326
Ervin MD (1951) Astraeus and Geastrum. In: proceedings of the iowa academy of science, vol. 58, No. 1, pp 97–99
Frohnhöfer HG, Krauss J, Maischein HM, Nüsslein-Volhard C (2013) Iridophores and their interactions with other chromatophores are required for stripe formation in zebrafish. Development 140:2997–3007
Gould SJ (1982) Change in developmental timing as a mechanism of macroevolution. In Evolution and development, Springer
Halbwachs H, Simmel J, Bässler C (2016) Tales and mysteries of fungal fruiting: how morphological and physiological traits affect a pileate lifestyle. Fungal Biol Rev 30(2):36–61
Hibbett DS (2007) After the gold rush, or before the flood? Evolutionary morphology of mushroom-forming fungi (Agaricomycetes) in the early 21st century. Mycol Res 111(9):1001–1018
Hibbett DS, Tsuneda A, Murakami S (1994) The secotioid form of Lentinus tigrinus: genetics and development of a fungal morphological innovation. Am J Bot 81(4):466–478
Hiscock TW, Megason SG (2015) Mathematically guided approaches to distinguish models of periodic patterning. Development 142:409–419
Jedd G (2011) Fungal evo–devo: organelles and multicellular complexity. Trends Cell Biol 21(1):12–19
Johnson BR, Lam SK (2010) Self-organization, natural selection, and evolution: cellular hardware and genetic software. Bioscience 60(11):879–885
Kinoshita A, Sasaki H, Nara K (2012) Multiple origins of sequestrate basidiomes within Entoloma inferred from molecular phylogenetic analysis. Fungal Biol 116:1250e1262
Kondo S (2017) An updated kernel-based Turing model for studying the mechanisms of biological pattern formation. J Theor Biol 414:120–127
Kondo S, Asal R (1995) A reaction-diffusion wave on the skin of the marine angelfish Pomacanthus. Nature 376:765–768
Kondo S, Miura T (2010) Reaction-diffusion model as a framework for understanding biological pattern formation. Science 329:1616–1620
Krizsán K, Almási É, Merényi Z, Sahu N, Virágh M, Kószó T, Mondo S, Kiss B, Bálint B, Kües U, Barry K (2019) Transcriptomic atlas of mushroom development reveals conserved genes behind complex multicellularity in fungi. PNAS 116(15):7409–7418
Kües U (2000) Life history and developmental processes in the basidiomycete Coprinus cinereus. Microbiol Mol Biol Rev 64(2):316–353
Kües U, Navarro-González M (2015) How do Agaricomycetes shape their fruiting bodies? 1 Morphological aspects of development. Fungal Biol Rev 29(2):63–97
Linde-Medina M (2020) On the problem of biological form. Theor Biosci 139(30):299–308
Liu QX, Doelman A, Rottschäfer V, de Jager M, Herman PM, Rietkerk M, van de Koppel J (2013) Phase separation explains a new class of self-organized spatial patterns in ecological systems. Proc Natl Acad Sci 110(29):11905–11910
Matheny PB, Curtis JM, Hofstetter V, Aime MC, Moncalvo JM, Ge ZW, Hibbett DS (2006) Major clades of Agaricales: a multilocus phylogenetic overview. Mycologia 98(6):982–995
McMeekin D (2000) Indole-3-acetic acid, glucose, and inoculum influence the formation and distribution of basidiocarps of Pholiota malicola in culture. Mycologia. 92:772–776
Meinhardt H (1982) Models of biological pattern formation. Academic Press
Meinhardt H (2012) Turing’s theory of morphogenesis of 1952 and the subsequent discovery of the crucial role of local self-enhancement and long-range inhibition. Interface Focus 2(4):407–416
Menshykau D, Blanc P, Unal E, Sapin V, Iber D (2014) An interplay of geometry and signaling enables robust lung branching morphogenesis. Development 141:4526–4536
Mercker M, Hartmann D, Marciniak-Czochra A (2013) A mechanochemical model for embryonic pattern formation: coupling tissue mechanics and morphogen expression. PloS one 8(12):e82617
Mercker M, Brinkmann F, Marciniak-Czochra A, Richter T (2016) Beyond Turing: mechanochemical pattern formation in biological tissues. Biol Direct 11(1):1–15
Meškauskas A, McNulty LJ, Moore D (2004) Concerted regulation of all hyphal tips generates fungal fruit body structures: experiments with computer visualizations produced by a new mathematical model of hyphal growth. Mycol Res 108(4):341–353
Miettinen O, Spirin V, Vlasák J, Rivoire B, Stenroos S, Hibbett D (2016) Polypores and genus concepts in phanerochaetaceae (Polyporales, Basidiomycota). MycoKeys 17:1
Miller OK Jr, Stewart L (1971) The genus Lentinellus. Mycologia 63(2):333–369
Mitteroecker P, Huttegger SM (2009) The concept of morphospaces in evolutionary and developmental biology: mathematics and metaphors. Biol Theory 4(1):54–67
Moore D, Wai Chiu S, Halit Umar M, Sánchez C (1998) In the midst of death we are in life: further advances in the study of higher fungi. Bot J Scotl 50(2):121–135
Moore D, McNulty LJ, Meškauskas A (2005). Branching in fungal hyphae and fungal tissues. In: branching morphogenesis (pp 75–90). Springer, Boston, MA
Mou C, Jackson B, Schneider P, Overbeek PA, Headon DJ (2006) Generation of the primary hair follicle pattern. Proc Natl Acad Sci 103(24):9075–9080
Moure A, Gomez H (2021) Phase-field modeling of individual and collective cell migration. Arch Comput Methods Eng 28(2):311–344
Mukherjee N, Ghorai S, Banerjee M (2019) Cross-diffusion induced Turing and non-Turing patterns in rosenzweig–MacArthur model. Lett Biomath 6(1):1–22
Murray JD, Oster GF (1984) Generation of biological pattern and form. Math Med Biol J IMA 1(1):51–75
Nagy LG, Kovács GM, Krizsán K (2018) Complex multicellularity in fungi: evolutionary convergence, single origin, or both? Biol Rev 93(4):1778–1794
Nagy LG, Tóth R, Kiss E, Slot J, Gácser A, Kovács GM (2017) Six key traits of fungi: their evolutionary origins and genetic bases. Microbiol Spectr. https://doi.org/10.1128/microbiolspec.FUNK-0036-2016
Nakamasu A, Takahashi G, Kanbe A, Kondo S (2009) Interactions between zebrafish pigment cells responsible for the generation of Turing patterns. Proc Natl Acad Sci USA 106:8429–8434
Nukina M, Ikeda M, Sassa T (1980) Two new pyrenolides, fungal morphogenic substances produced by Pyrenophora teres (Diedicke) Drechsler. Agric Biol Chem 44(11):2761–2762
Odell GM, Oster G, Alberch P, Burnside B (1981) The mechanical basis of morphogenesis: I epithelial folding and invagination. Develop Biol 85(2):446–462
Oster GF, Murray JD, Harris AK (1983) Mechanical Aspects of Mesenchymal Morphogenesis. Development 78(1):83–125
Prigogine I, Stengers I (1984) Order out of chaos: Man’s new dialogue with nature. Bantam, New York
Rayner AD, Griffith GS, Wildman HG (1994) Induction of metabolic and morphogenetic changes during mycelial interactions among species of higher fungi. Biochem Soc Trans 22(2):389–393
Rayner ADM, Watkins ZR, Beeching JR (1999) Self-integration–an emerging concept from the fungal mycelium. The fungal colony, 1–24
Ryvarden L. 2016. Neotropical Polypores Part 3 - Polyporaceae: Obba - Wrightoporia. Synopsis Fungorum 36. Fungiflora, Oslo, Norway
Scholes NS, Schnoerr D, Isalan M, Stumpf M (2019) A comprehensive network atlas reveals that Turing patterns are common but not robust. Cell Syst 9(3):243–257
Schweisguth F, Corson F (2019) Self-organization in pattern formation. Dev Cell 49(5):659–677
Sheth R, Grégoire D, Dumouchel A, Scotti M, Pham JMT, Nemec S, Bastida MF, Ros MA, Kmita M (2013) Decoupling the function of Hox and Shh in developing limb reveals multiple inputs of Hox genes on limb growth. Development 140:2130–2138
Shyer AE, Tallinen T, Nerurkar NL, Wei Z, Gil ES, Kaplan DL, Tabin CJ, Mahadevan L (2013) Villification: how the gut gets its villi. Science 342:212–218
Siber A, Ziherl P (2017) Cellular Patterns. CRC Press
Sick S, Reinker S, Timmer J, Schlake T (2006) WNT and DKK determine hair follicle spacing through a reaction-diffusion mechanism. Science 314(5804):1447–1450
Sjokvist E, Larsson E, Eberhardt U, Ryvarden L, Larsson K-H (2012) Stipitate steroid basidiocarps have evolved multiple times. Mycologia 104:1046e1055
Stayton CT (2015) What does convergent evolution mean? The interpretation of convergence and its implications in the search for limits to evolution. Interface Focus 5(6):20150039
Taber LA (1995) Biomechanics of growth, remodeling, and morphogenesis. Appl Mech Rev 48(8):487–545
Turing AM (1952) The chemical basis of morphogenesis. Bull Math Biol 52(1–2):153–197
Ugalde U, Rodriguez-Urra AB (2016). 9 Autoregulatory Signals in Mycelial Fungi. In Growth, Differentiation and Sexuality. Springer, Cham, pp. 185–202
Varga T, Krizsán K, Földi C, Dima B, Sánchez-García M, Sánchez-Ramírez S, Szöllősi GJ, Szarkándi JG, Papp V, Albert L, Andreopoulos W, Angelini C, Antonín V, Barry KW, Bougher NL, Buchanan P, Buyck B, Bense V, Catcheside P, Chovatia M, Cooper J, Dämon W, Desjardin D, Finy P, Geml J, Haridas S, Hughes K, Justo A, Karasiński D, Kautmanova I, Kiss B, Kocsubé S, Kotiranta H, LaButti KM, Lechner BE, Liimatainen K, Lipzen A, Lukács Z, Mihaltcheva S, Morgado LN, Niskanen T, Noordeloos ME, Ohm RA, Ortiz-Santana B, Ovrebo C, Rácz N, Riley R, Savchenko A, Shiryaev A, Soop K, Spirin V, Szebenyi C, Tomšovský M, Tulloss RE, Uehling J, Grigoriev IV, Vágvölgyi C, Papp T, Martin FM, Miettinen O, Hibbet DS, Nagy LG (2019) Megaphylogeny resolves global patterns of mushroom evolution. Nat Ecol Evolut 3(4):668–678
Varga T, Földi C, Bense V, Nagy LG (2021) Developmental innovations promote species diversification in mushroom-forming fungi. bioRxiv. https://doi.org/10.1101/2021.03.10.434564
Wake DB (1991) Homoplasy: the result of natural selection, or evidence of design limitations? Am Nat 138(3):543–567
Whitney KD, Arnott HJ (1986) Calcium oxalate crystals and basidiocarp dehiscence in Geastrum saccatum (Gasteromycetes). Mycologia 78(4):649–656
Wilson AW, Binder M, Hibbett DS (2011) Effects of gasteroid fruiting body morphology on diversification rates in three independent clades of fungi estimated using binary state speciation and extinction analysis. Evol Int J Org Evol 65(5):1305–1322
Wu B, Xu Z, Knudson A, Carlson A, Chen N, Kovaka S, Schakwitz W (2018) Genomics and development of Lentinus tigrinus: a white-rot wood-decaying mushroom with dimorphic fruiting bodies. Genome Biol Evol 10(12):3250–3261
Yamaguchi M, Yoshimoto E, Kondo S (2007) Pattern regulation in the stripe of zebrafish suggests an underlying dynamic and autonomous mechanism. Proc Natl Acad Sci USA 104:4790–4793
Yin J, Yagüe JL, Eggenspieler D, Gleason KK, Boyce MC (2012) Deterministic order in surface micro-topologies through sequential wrinkling. Adv Mater 24(40):5441–5446
Yoo PJ, Park SY, Kwon SJ, Suh KY, Lee HH (2003) Microshaping metal surfaces by wave-directed self-organization. Appl Phys Lett 83(21):4444–4446
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The authors thank Alejandro Sequeira for his invaluable help with the artwork and images, Michael Weese, who also provided an image and Juan Pablo Toribio for proofreading the manuscript. The financial support was provided by FONCyT (Grant PICT 2018-3781 to FK) and CONICET.
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The form is not encoded; what is encoded is the developmental path that leads to it Siber & Ziherl 2017.
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Kuhar, F., Terzzoli, L., Nouhra, E. et al. Pattern formation features might explain homoplasy: fertile surfaces in higher fungi as an example. Theory Biosci. 141, 1–11 (2022). https://doi.org/10.1007/s12064-022-00363-z
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DOI: https://doi.org/10.1007/s12064-022-00363-z