Abstract
Key message
Most known phytohormones regulate moss development. We present a comprehensive view of the synthesis and signaling pathways for the most investigated of these compounds in mosses, focusing on the model Physcomitrium patens.
Abstract
The last 50 years of research have shown that most of the known phytohormones are synthesized by the model moss Physcomitrium patens (formerly Physcomitrella patens) and regulate its development, in interaction with responses to biotic and abiotic stresses. Biosynthesis and signaling pathways are best described in P. patens for the three classical hormones auxins, cytokinins and abscisic acid. Furthermore, their roles in almost all steps of development, from early filament growth to gametophore development and sexual reproduction, have been the focus of much research effort over the years. Evidence of hormonal roles exist for ethylene and for CLE signaling peptides, as well as for salicylic acid, although their possible effects on development remain unclear. Production of brassinosteroids by P. patens is still debated, and modes of action for these compounds are even less known. Gibberellin biosynthesis and signaling may have been lost in P. patens, while gibberellin precursors such as ent-kaurene derivatives could be used as signals in a yet to discover pathway. As for jasmonic acid, it is not used per se as a hormone in P. patens, but its precursor OPDA appears to play a corresponding role in defense against abiotic stress. We have tried to gather a comprehensive view of the biosynthesis and signaling pathways for all these compounds in mosses, without forgetting strigolactones, the last class of plant hormones to be reported. Study of the strigolactone response in P. patens points to a novel signaling compound, the KAI2-ligand, which was likely employed as a hormone prior to land plant emergence.
Similar content being viewed by others
References
Abel WO, Knebel W, Koop H-U, Marienfeld JR, Quader H, Reski R, Schnepf E, Spörlein B (1989) A cytokinin-sensitive mutant of the moss, Physcomitrella patens, defective in chloroplast division. Protoplasma 152:1–13
Achard P, Genschik P (2009) Releasing the brakes of plant growth: how GAs shutdown DELLA proteins. J Exp Bot 60:1085–1092
Al-Babili S, Bouwmeester HJ (2015) Strigolactones, a novel carotenoid-derived plant hormone. Annu Rev Plant Biol 66:161–186
Amagai A, Honda Y, Ishikawa S, Hara Y, Kuwamura M, Shinozawa A, Sugiyama N, Ishihama Y, Takezawa D, Sakata Y, Shinozaki K, Umezawa T (2018) Phosphoproteomic profiling reveals ABA-responsive phosphosignaling pathways in Physcomitrella patens. Plant J 94:699–708
Anterola A, Göbel C, Hornung E, Sellhorn G, Feussner I, Grimes H (2009a) Physcomitrella patens has lipoxygenases for both eicosanoid and octadecanoid pathways. Phytochemistry 70:40–52
Anterola A, Shanle E, Mansouri K, Schuette S, Renzaglia K (2009b) Gibberellin precursor is involved in spore germination in the moss Physcomitrella patens. Planta 229:1003–1007
Aoyama T, Hiwatashi Y, Shigyo M, Kofuji R, Kubo M, Ito M, Hasebe M (2012) AP2-type transcription factors determine stem cell identity in the moss Physcomitrella patens. Development 139:3120–3129
Arif MA, Hiss M, Tomek M, Busch H, Meyberg R, Tintelnot S, Reski R, Rensing SA, Frank W (2019) ABA-induced vegetative diaspore formation in Physcomitrella patens. Front Plant Sci 10:1–18
Ashton NW, Cove DJ (1977) The isolation and preliminary characterisation of auxotrophic and analogue resistant mutants of the moss, Physcomitrella patens. Mol Gen Genet 154:87–95
Ashton NW, Cove DJ, Featherstone DR (1979a) The isolation and physiological analysis of mutants of the moss, Physcomitrella patens, which over-produce gametophores. Planta 144:437–442
Ashton NW, Grimsley NH, Cove DJ (1979b) Analysis of gametophytic development in the moss, Physcomitrella patens, using auxin and cytokinin resistant mutants. Planta 144:427–435
Asprey GF, Benson-Evans K, Lyon AG (1958) Effect of gibberellin and lndoleacetic acid on seta elongation in Pellia epiphylla. Nature 181:1351
Axtell MJ, Snyder JA, Bartel DP (2007) Common functions for diverse small RNAs of land plants. Plant Cell 19:1750–1769
Bandara PKGSS, Takahashi K, Sato M, Matsuura H, Nabeta K (2009) Cloning and functional analysis of an allene oxide synthase in Physcomitrella patens. Biosci Biotechnol Biochem 73:2356–2359
Bennett TA et al (2014) Plasma membrane-targeted PIN proteins drive shoot development in a moss. Curr Biol 24:2776–2785
Blázquez MA, Nelson DC, Weijers D (2020) Evolution of plant hormone response pathways. Annu Rev Plant Biol 71:327–353
Bopp M (1968) Control of differentiation in fern-allies and bryophytes. Annu Rev Plant Physiol 19:361–380
Bopp M, Werner O (1993) Abscisic acid and desiccation tolerance in mosses. Bot Acta 106:103–106
Bowman JL et al (2017) Insights into land plant evolution garnered from the Marchantia polymorpha genome. Cell 171:287-304.e15
Bowman JL, Briginshaw LN, Fisher TJ, Flores-Sandoval E (2019) Something ancient and something neofunctionalized—evolution of land plant hormone signaling pathways. Curr Opin Plant Biol 47:64–72
Brandes H, Kende H (1968) Studies on cytokinin-controlled bud formation in moss Protonemata. Plant Physiol 43:827–837
Breithaupt C, Kurzbauer R, Schaller F, Stintzi A, Schaller A, Huber R, Macheroux P, Clausen T (2009) Structural basis of substrate specificity of plant 12-oxophytodienoate reductases. J Mol Biol 392:1266–1277
Bressendorff S, Azevedo R, Kenchappa CS, Ponce de León I, Olsen JV, Rasmussen MW, Erbs G, Newman MA, Petersen M, Mundy J (2016) An innate immunity pathway in the moss Physcomitrella patens. Plant Cell 28:1328–1342
Briones-Moreno A, Hernández-García J, Vargas-Chávez C, Romero-Campero FJ, Romero JM, Valverde F, Blázquez MA (2017) Evolutionary analysis of DELLA-associated transcriptional networks. Front Plant Sci 8:1–11
Bürger M, Mashiguchi K, Lee HJ, Nakano M, Takemoto K, Seto Y, Yamaguchi S, Chory J (2019) Structural basis of karrikin and non-natural strigolactone perception in Physcomitrella patens. Cell Rep 26:855-865.e5
Bythell-Douglas R, Rothfels CJ, Stevenson DWD, Graham SW, Wong GK-S, Nelson DC, Bennett T (2017) Evolution of strigolactone receptors by gradual neo-functionalization of KAI2 paralogues. BMC Biol 15:52
Cammarata J, Roeder AH, Scanlon MJ (2019) Cytokinin and CLE signaling are highly intertwined developmental regulators across tissues and species. Curr Opin Plant Biol 51:96–104
Cannell N, Emms DM, Hetherington AJ, MacKay J, Kelly S, Dolan L, Sweetlove LJ (2020) Multiple metabolic innovations and losses are associated with major transitions in land plant evolution. Curr Biol 30:1783–1800
Causier B, Lloyd J, Stevens L, Davies B (2012) TOPLESS co-repressor interactions and their evolutionary conservation in plants. Plant Signal Behav 7:1–4
Chang KN et al (2013) Temporal transcriptional response to ethylene gas drives growth hormone cross-regulation in Arabidopsis. Elife 2013:1–20
Chater C, Kamisugi Y, Movahedi M, Fleming A, Cuming AC, Gray JE, Beerling DJ (2011) Regulatory mechanism controlling stomatal behavior conserved across 400 million years of land plant evolution. Curr Biol 21:1025–1029
Cheon J, Fujioka S, Dilkes BP, Choe S (2013) Brassinosteroids regulate plant growth through distinct signaling pathways in Selaginella and Arabidopsis. PLoS ONE 8:e81938
Chico JM, Chini A, Fonseca S, Solano R (2008) JAZ repressors set the rhythm in jasmonate signaling. Curr Opin Plant Biol 11:486–494
Chopra RN, Gupta U (1967) Dark-induction of buds in Funaria hygrometrica Hedw. Bryologist 70:102–104
Christianson ML (1998) The quantitative response to cytokinin in the moss Funaria hygrometrica does not reflect differential sensitivity of initial target cells. Am J Bot 85:144–148
Christianson ML (2000) ABA prevents the second cytokinin-mediated event during the induction of shoot buds in the moss Funaria hygrometrica. Am J Bot 87:1540–1545
Christianson ML, Duffy SH (2002) Dose-dependent effect of salicylates in a moss, Funaria Hygrometrica. J Plant Growth Regul 21:200–208
Cooke TJ, Poli D, Sztein AE, Cohen JD (2002) Evolutionary patterns in auxin action. Plant Mol Biol 49:319–338
Coudert Y, Palubicki W, Ljung K, Novak O, Leyser O, Harrison CJ (2015) Three ancient hormonal cues co-ordinate shoot branching in a moss. Elife 4:1–26
Cove D, Bezanilla M, Harries P, Quatrano R (2006) Mosses as model systems for the study of metabolism and development. Annu Rev Plant Biol 57:497–520
Cuming AC (2019) Evolution of ABA signaling pathways. Adv Bot Res 92:281–313
Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61:651–679
Davidson SE, Reid JB, Helliwell CA (2006) Cytochromes P450 in gibberellin biosynthesis. Phytochem Rev 5:405–419
Daviere J-M, Achard P (2013) Gibberellin signaling in plants. Development 140:1147–1151
de Vries S, de Vries J, von Dahlen JK, Gould SB, Archibald JM, Rose LE, Slamovits CH (2018) On plant defense signaling networks and early land plant evolution. Commun Integr Biol 11:1–14
Decker EL, Frank W, Sarnighausen E, Reski R (2006) Moss systems biology en route: phytohormones in Physcomitrella development. Plant Biol 8:397–406
Decker EL et al (2017) Strigolactone biosynthesis is evolutionarily conserved, regulated by phosphate starvation and contributes to resistance against phytopathogenic fungi in a moss, Physcomitrella patens. New Phytol 216:455–468
Delaux PM, Xie X, Timme RE, Puech-Pages V, Dunand C, Lecompte E, Delwiche CF, Yoneyama K, Bécard G, Séjalon-Delmas N (2012) Origin of strigolactones in the green lineage. New Phytol 195:857–871
Ding Y, Sun T, Ao K, Peng Y, Zhang Y, Li X, Zhang Y (2018) Opposite roles of salicylic acid receptors NPR1 and NPR3/NPR4 in transcriptional regulation of plant immunity. Cell 173:1454–1467
Doonan JH, Cove DJ, Corke FMK, Lloyd CW (1987) Pre-prophase band of microtubules, absent from tip-growing moss filaments, arises in leafy shoots during transition to intercalary growth. Cell Motil Cytoskeleton 7:138–153
Drábková LZ, Dobrev PI, Motyka V (2015) Phytohormone profiling across the bryophytes. PLoS ONE 10:1–19
Dubois M, Van den Broeck L, Inzé D (2018) The pivotal role of ethylene in plant growth. Trends Plant Sci 23:311–323
Eklund DM, Thelander M, Landberg K, Ståldal V, Nilsson A, Johansson M, Valsecchi I, Pederson ERA, Kowalczyk M, Ljung K, Ronne H, Sundberg E (2010) Homologues of the Arabidopsis thaliana SHI/STY/LRP1 genes control auxin biosynthesis and affect growth and development in the moss Physcomitrella patens. Development 137:1275–1284
Engel PP (1968) The induction of biochemical and morphological mutants in the moss Physcomitrella patens. Am J Bot 55:438–446
Fesenko I et al (2019) Phytohormone treatment induces generation of cryptic peptides with antimicrobial activity in the moss Physcomitrella patens. BMC Plant Biol 19:1–16
Filippova A, Lyapina I, Kirov I, Zgoda V, Belogurov A, Kudriaeva A, Ivanov V, Fesenko I (2019) Salicylic acid influences the protease activity and posttranslation modifications of the secreted peptides in the moss physcomitrella patens. J Pept Sci 25:1–11
Finet C, Jaillais Y (2012) Auxology: when auxin meets plant evo-devo. Dev Biol 369:19–31
Finkelstein R (2013) Abscisic acid synthesis and response. Arab B 11:e0166
Flematti GR, Ghisalberti EL, Dixon KW, Trengove RD (2004) A compound from smoke that promotes seed germination. Science 305:977
Fletcher JC (2020) Recent advances in arabidopsis CLE peptide signaling. Trends Plant Sci 25:1005–1016
Frébort I, Kowalska M, Hluska T, Frébortová J, Galuszka P (2011) Evolution of cytokinin biosynthesis and degradation. J Exp Bot 62:2431–2452
Fujita T, Sakaguchi H, Hiwatashi Y, Wagstaff SJ, Ito M, Deguchi H, Sato T, Hasebe M (2008) Convergent evolution of shoots in land plants: lack of auxin polar transport in moss shoots. Evol Dev 10:176–186
Ghorbani S (2014) Signaling peptides in plants. Cell Dev Biol 03:98–101
Goad DM, Zhu C, Kellogg EA (2017) Comprehensive identification and clustering of CLV3/ESR-related (CLE) genes in plants finds groups with potentially shared function. New Phytol 216:605–616
Goode JA, Alfano F, Stead AD, Duckett JG (1993a) The formation of aplastidic abscission (tmema) cells and protonemal disruption in the moss Bryum tenuisetum Limpr. is associated with transverse arrays of microtubules and microfilaments. Protoplasma 174:158–172
Goode JA, Stead AD, Duckett JG (1993b) Redifferentiation of moss protonemata: an experimental and immunofluorescence study of brood cell formation. Can J Bot 71:1510–1519
Gorton BS, Eakin RE (1957) Development of the gametophyte in the moss Tortella caespitosa. Bot Gaz 119:31–38
Gruhn N, Heyl A (2013) Updates on the model and the evolution of cytokinin signaling. Curr Opin Plant Biol 16:569–574
Gruhn N, Halawa M, Snel B, Seidl MF, Heyl A (2014) A subfamily of putative cytokinin receptors is revealed by an analysis of the evolution of the two-component signaling system of plants. Plant Physiol 165:227–237
Gu R, Fu J, Guo S, Duan F, Wang Z, Mi G, Yuan L (2010) Comparative expression and phylogenetic analysis of maize cytokinin dehydrogenase/oxidase (CKX) gene family. J Plant Growth Regul 29:428–440
Han GZ (2017) Evolution of jasmonate biosynthesis and signalling mechanisms. J Exp Bot 68:1323–1331
Hashimoto T, Takahashi K, Sato M, Bandara PKGSS, Nabeta K (2011) Cloning and characterization of an allene oxide cyclase, PpAOC3, in Physcomitrella patens. Plant Growth Regul 65:239–245
Hayashi K, Kawaide H, Notomi M, Sakigi Y, Matsuo A, Nozaki H (2006) Identification and functional analysis of bifunctional ent-kaurene synthase from the moss Physcomitrella patens. FEBS Lett 580:6175–6181
Hayashi KI, Horie K, Hiwatashi Y, Kawaide H, Yamaguchi S, Hanada A, Nakashima T, Nakajima M, Mander LN, Yamane H, Hasebe M, Nozaki H (2010) Endogenous diterpenes derived from ent-kaurene, a common gibberellin precursor, regulate protonema differentiation of the moss Physcomitrella patens. Plant Physiol 153:1085–1097
Hedden P, Phillips AL, Rojas MC, Carrera E, Tudzynski B (2001) Gibberellin biosynthesis in plants and fungi: a case of convergent evolution? J Plant Growth Regul 20:319–331
Hernández-García J, Briones-Moreno A, Dumas R, Blázquez MA (2019) Origin of Gibberellin-dependent transcriptional regulation by molecular exploitation of a transactivation domain in DELLA proteins. Mol Biol Evol 36:908–918
Hirano K et al (2007) The GID1-mediated gibberellin perception mechanism is conserved in the lycophyte Selaginella moellendorffii but not in the bryophyte Physcomitrella patens. Plant Cell 19:3058–3079
Hoffmann B, Proust H, Belcram K, Labrune C, Boyer FD, Rameau C, Bonhomme S (2014) Strigolactones inhibit caulonema elongation and cell division in the moss Physcomitrella patens. PLoS ONE 9:1–10
Huang H, Liu B, Liu L, Song S (2017) Jasmonate action in plant growth and development. J Exp Bot 68:1349–1359
Hyoung S, Cho SH, Chung JH, So WM, Cui MH, Shin JS (2020) Cytokinin oxidase PpCKX1 plays regulatory roles in development and enhances dehydration and salt tolerance in Physcomitrella patens. Plant Cell Rep 39:419–430
Imaizumi T, Kadota A, Hasebe M, Wada M (2002) Cryptochrome light signals control development to suppress auxin sensitivity in the moss Physcomitrella patens. Plant Cell 14:373–386
Iqbal N, Khan NA, Ferrante A, Trivellini A, Francini A, Khan MIR (2017) Ethylene role in plant growth, development and senescence: interaction with other phytohormones. Front Plant Sci 08:1–19
Ishida K, Yamashino T, Nakanishi H, Mizuno T (2010) Classification of the genes involved in the two-component system of the moss Physcomitrella patens. Biosci Biotechnol Biochem 74:2542–2545
Jahan A, Komatsu K, Wakida-Sekiya M, Hiraide M, Tanaka K, Ohtake R, Umezawa T, Toriyama T, Shinozawa A, Yotsui I, Sakata Y, Takezawa D (2019) Archetypal roles of an abscisic acid receptor in drought and sugar responses in liverworts. Plant Physiol 179:317–328
Jang G, Dolan L (2011) Auxin promotes the transition from chloronema to caulonema in moss protonema by positively regulating PpRSL1and PpRSL2 in Physcomitrella patens. New Phytol 192:319–327
Johri MM, Desai S (1973) Auxin regulation of caulonema formation in moss protonema. Nat New Biol 245:223–224
Ju C, Van de Poel B, Cooper ED, Thierer JH, Gibbons TR, Delwiche CF, Chang C (2015) Conservation of ethylene as a plant hormone over 450 million years of evolution. Nat Plants 1:14004
Kamisugi Y, Cuming AC (2005) The evolution of the abscisic acid-response in land plants: comparative analysis of group 1 LEA gene expression in moss and cereals. Plant Mol Biol 59:723–737
Kato H, Nishihama R, Weijers D, Kohchi T (2017) Evolution of nuclear auxin signaling: lessons from genetic studies with basal land plants. J Exp Bot 69:1–11
Kawai Y, Ono E, Mizutani M (2014) Evolution and diversity of the 2-oxoglutarate-dependent dioxygenase superfamily in plants. Plant J 78:328–343
Khandelwal A, Cho SH, Marella H, Sakata Y, Perroud PF, Pan A, Quatrano RS (2010) Role of ABA and ABI3 in desiccation tolerance. Science 327:546
Kieber JJ, Schaller GE (2018) Cytokinin signaling in plant development. Development 145:149344
Komatsu K, Nishikawa Y, Ohtsuka T, Taji T, Quatrano RS, Tanaka S, Sakata Y (2009) Functional analyses of the ABI1-related protein phosphatase type 2C reveal evolutionarily conserved regulation of abscisic acid signaling between Arabidopsis and the moss Physcomitrella patens. Plant Mol Biol 70:327–340
Komatsu K, Suzuki N, Kuwamura M, Nishikawa Y, Nakatani M, Ohtawa H, Takezawa D, Seki M, Tanaka M, Taji T, Hayashi T, Sakata Y (2013) Group A PP2Cs evolved in land plants as key regulators of intrinsic desiccation tolerance. Nat Commun 4:1–7
Kwiatkowska M, Wojtczak A, Popłońska K (1998) Effect of GA3 treatment on the number of spermatozoids and endopolyploidy levels of non-generative cells in antheridia of Chara vulgaris L. Plant Cell Physiol 39:1388–1390
Landberg K, Pederson ERA, Viaene T, Bozorg B, Friml J, Jönsson H, Thelander M, Sundberg E (2013) The moss Physcomitrella patens reproductive organ development is highly organized, affected by the two SHI/STY genes and by the level of active auxin in the SHI/STY expression domain. Plant Physiol 162:1406–1419
Lavy M, Prigge MJ, Tao S, Shain S, Kuo A, Kirchsteiger K, Estelle M (2016) Constitutive auxin response in Physcomitrella reveals complex interactions between Aux/IAA and ARF proteins. Elife 5:1–21
Lefevere H, Bauters L, Gheysen G (2020) Salicylic acid biosynthesis in plants. Front Plant Sci 11:1–7
Li W, Liu B, Yu L, Feng D, Wang H, Wang J (2009) Phylogenetic analysis, structural evolution and functional divergence of the 12-oxo-phytodienoate acid reductase gene family in plants. BMC Evol Biol 9:1–19
Li Z, Shen J, Liang J (2019) Genome-Wide identification, expression profile, and alternative splicing analysis of the brassinosteroid-signaling kinase (BSK) family genes in Arabidopsis. Int J Mol Sci 20:1138
Li D, Flores-Sandoval E, Ahtesham U, Coleman A, Clay JM, Bowman JL, Chang C (2020a) Ethylene-independent functions of the ethylene precursor ACC in Marchantia polymorpha. Nat Plants 6:1335–1344
Li F-W et al (2020b) Anthoceros genomes illuminate the origin of land plants and the unique biology of hornworts. Nat Plants 6:259–272
Lopez-Obando M, Hoffmann B, Gery C, Guyon-Debast A, Teoule E, Rameau C, Bonhomme S, Nogue F (2016) Simple and efficient targeting of multiple genes through CRISPR-Cas9 in Physcomitrella patens. G3 Genes Genomes Genet 6:3647–3653
Lopez-Obando M, de Villiers R, Hoffmann B, Ma L, de Saint Germain A, Kossmann J, Coudert Y, Harrison CJ, Rameau C, Hills P, Bonhomme S (2018) Physcomitrella patens MAX2 characterization suggests an ancient role for this F-box protein in photomorphogenesis rather than strigolactone signalling. New Phytol 219:743–756
Ludwig-Müller J, Jülke S, Bierfreund NM, Decker EL, Reski R (2009) Moss (Physcomitrella patens) GH3 proteins act in auxin homeostasis. New Phytol 181:323–338
Luo W, Nanjo Y, Komatsu S, Matsuura H, Takahashi K (2016) Proteomics of Physcomitrella patens protonemata subjected to treatment with 12-oxo-phytodienoic acid. Biosci Biotechnol Biochem 80:2357–2364
Luo W, Komatsu S, Abe T, Matsuura H, Takahashi K (2020) Comparative proteomic analysis of wild-type Physcomitrella patens and an OPDA-deficient Physcomitrella patens mutant with disrupted PpAOS1 and PpAOS2 genes after wounding. Int J Mol Sci 21:1417
Mallett DR, Chang M, Cheng X, Bezanilla M (2019) Efficient and modular CRISPR-Cas9 vector system for Physcomitrella patens. Plant Direct 3:1–15
Marella HH, Sakata Y, Quatrano RS (2006) Characterization and functional analysis of ABSCISIC ACID INSENSITIVE3-like genes from Physcomitrella patens. Plant J 46:1032–1044
Martin-Arevalillo R, Thévenon E, Jégu F, Vinos-Poyo T, Vernoux T, Parcy F, Dumas R (2019) Evolution of the auxin response factors from charophyte ancestors. PLoS Genet 15:e1008400
Matsui H, Iwakawa H, Hyon G-S, Yotsui I, Katou S, Monte I, Nishihama R, Franzen R, Solano R, Nakagami H (2020) Isolation of natural fungal pathogens from Marchantia polymorpha reveals antagonism between salicylic acid and jasmonate during liverwort–fungus interactions. Plant Cell Physiol 61:265–275
Minami A, Nagao M, Arakawa K, Fujikawa S, Takezawa D (2003) Abscisic acid-induced freezing tolerance in the moss Physcomitrella patens is accompanied by increased expression of stress-related genes. J Plant Physiol 160:475–483
Minami A, Nagao M, Arakawa K, Fujikawa S, Takezawa D (2006) Physiological and morphological alterations associated with development of freezing tolerance in the moss Physcomitrella patens. In: Chen T (ed) Cold hardiness in plants: molecular genetics, cell biology and physiology. CABI, Cambridge, pp 138–152
Mishra S, Upadhyay S, Shukla RK (2017) The role of strigolactones and their potential cross-talk under hostile ecological conditions in plants. Front Physiol 7:1–7
Miyazaki S, Toyoshima H, Natsume M, Nakajima M, Kawaide H (2014) Blue-light irradiation up-regulates the ent-kaurene synthase gene and affects the avoidance response of protonemal growth in Physcomitrella patens. Planta 240:117–124
Miyazaki S, Nakajima M, Kawaide H (2015) Hormonal diterpenoids derived from ent-kaurenoic acid are involved in the blue-light avoidance response of Physcomitrella patens. Plant Signal Behav 10:e989046
Miyazaki S, Hara M, Ito S, Tanaka K, Asami T et al (2018) An ancestral gibberellin in a moss Physcomitrella patens. Mol Plant 11:1097–1100
Modlin IM, Kidd M, Farhadi J (2000) Bayliss and Starling and the nascence of endocrinology. Regul Pept 93:109–123
Monte I et al (2018) Ligand-receptor co-evolution shaped the jasmonate pathway in land plants. Nat Chem Biol 14:480–488
Moody LA, Saidi Y, Gibbs DJ, Choudhary A, Holloway D, Vesty EF, Bansal KK, Bradshaw SJ, Coates JC (2016) An ancient and conserved function for Armadillo-related proteins in the control of spore and seed germination by abscisic acid. New Phytol 211:940–951
Moore TC (2012) Biochemistry and physiology of plant hormones. Springer, New York
Morffy N, Strader LC (2020) Old town roads: routes of auxin biosynthesis across kingdoms. Curr Opin Plant Biol 55:21–27
Morikawa T, Saga H, Hashizume H, Ohta D (2009) CYP710A genes encoding sterol C22-desaturase in Physcomitrella patens as molecular evidence for the evolutionary conservation of a sterol biosynthetic pathway in plants. Planta 229:1311–1322
Moturu TR, Thula S, Singh RK, Nodzyński T, Vařeková RS, Friml J, Simon S (2018) Molecular evolution and diversification of the SMXL gene family. J Exp Bot 69:2367–2378
Nagao M, Minami A, Arakawa K, Fujikawa S, Takezawa D (2005) Rapid degradation of starch in chloroplasts and concomitant accumulation of soluble sugars associated with ABA-induced freezing tolerance in the moss Physcomitrella patens. J Plant Physiol 162:169–180
Nolan TM, Vukašinović N, Liu D, Russinova E, Yin Y (2020) Brassinosteroids: multidimensional regulators of plant growth, development, and stress responses. Plant Cell 32:295–318
Nyman LP, Cutter EG (1981) Auxin–cytokinin interaction in the inhibition, release, and morphology of gametophore buds of Plagiomnium cuspidatum from apical dominance. Can J Bot 59:750–762
Oliver MJ, Velten J, Mishler BD (2005) Desiccation tolerance in bryophytes: a reflection of the primitive strategy for plant survival in dehydrating habitats? Integr Comp Biol 45:788–799
Oliver JP, Castro A, Gaggero C, Cascón T, Schmelz EA, Castresana C, Ponce De León I (2009) Pythium infection activates conserved plant defense responses in mosses. Planta 230:569–579
Olsson T, Thelander M, Ronne H (2003) A novel type of chloroplast stromal hexokinase is the major glucose-phosphorylating enzyme in the moss Physcomitrella patens. J Biol Chem 278:44439–44447
Paponov IA, Teale W, Lang D, Paponov M, Reski R, Rensing SA, Palme K (2009) The evolution of nuclear auxin signalling. BMC Evol Biol 9:1–16
Park J, Lee Y, Martinoia E, Geisler M (2017) Plant hormone transporters: what we know and what we would like to know. BMC Biol 15:1–15
Peng Y, Sun T, Zhang Y (2017) Perception of salicylic acid in Physcomitrella patens. Front Plant Sci 8:1–5
Pils B, Heyl A (2009) Unraveling the evolution of cytokinin signaling. Plant Physiol 151:782–791
Plavskin Y, Nagashima A, Perroud P-F, Hasebe M, Quatrano RS, Atwal GS, Timmermans MCP (2016) Ancient trans-acting siRNAs confer robustness and sensitivity onto the auxin response. Dev Cell 36:276–289
Ponce de León I, Schmelz EA, Gaggero C, Castro A, Álvarez A, Montesano M (2012) Physcomitrella patens activates reinforcement of the cell wall, programmed cell death and accumulation of evolutionary conserved defence signals, such as salicylic acid and 12-oxo-phytodienoic acid, but not jasmonic acid, upon Botrytis cinerea infection. Mol Plant Pathol 13:960–974
Ponce de León I, Hamberg M, Castresana C (2015) Oxylipins in moss development and defense. Front Plant Sci 6:1–12
Pressel S, Duckett JG (2010) Cytological insights into the desiccation biology of a model system: moss protonemata. New Phytol 185:944–963
Prigge MJ, Lavy M, Ashton NW, Estelle M (2010) Physcomitrella patens auxin-resistant mutants affect conserved elements of an auxin-signaling pathway. Curr Biol 20:1907–1912
Proust H, Hoffmann B, Xie X, Yoneyama K, Schaefer DG, Yoneyama K, Nogue F, Rameau C (2011) Strigolactones regulate protonema branching and act as a quorum sensing-like signal in the moss Physcomitrella patens. Development 138:1531–1539
Quatrano R, McDaniel SF, Khandelwal A, Perroud P-F, Cove DJ (2007) Physcomitrella patens: mosses enter the genomic age. Curr Opin Plant Biol 10:182–189
Qudeimat E, Faltusz AMC, Wheeler G, Lang D, Holtorf H, Brownlee C, Reski R, Frank W (2008) A PIIB-type Ca2+-ATPase is essential for stress adaptation in Physcomitrella patens. Proc Natl Acad Sci 105:19555–19560
Rensing SA et al (2008) The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319:64–69
Rensing SA, Goffinet B, Meyberg R, Wu S-Z, Bezanilla M (2020) The moss Physcomitrium (Physcomitrella) patens: a model organism for non-seed plants. Plant Cell 32:1361–1376
Reski R, Abel WO (1985) Induction of budding on chloronemata and caulonemata of the moss, Physcomitrella patens, using isopentenyladenine. Planta 165:354–358
Reski R, Wehe M, Hadeler B, Marienfeld JR, Abel WO (1991) Cytokinin and light quality interact at the molecular level in the chloroplast-mutant PC22 of the moss Physcomitrella. J Plant Physiol 138:236–243
Reutter K, Atzorn R, Hadeler B, Schmülling T, Reski R (1998) Expression of the bacterial ipt gene in Physcomitrella rescues mutations in budding and in plastid division. Planta 206:196–203
Richardt S, Timmerhaus G, Lang D, Qudeimat E, Corrêa LGG, Reski R, Rensing SA, Frank W (2010) Microarray analysis of the moss Physcomitrella patens reveals evolutionarily conserved transcriptional regulation of salt stress and abscisic acid signalling. Plant Mol Biol 72:27–45
Richter H, Lieberei R, Strnad M, Novák O, Gruz J, Rensing SA, von Schwartzenberg K (2012) Polyphenol oxidases in Physcomitrella: functional PPO1 methylation and chromatin patterning knockout modulates cytokinin-dependent development in the moss Physcomitrella patens. J Exp Bot 63:5121–5135
Rohwer F, Bopp M (1985) Ethylene synthesis in moss protonema. J Plant Physiol 117:331–338
Ross JJ, Reid JB (2010) Evolution of growth-promoting plant hormones. Funct Plant Biol 37:795
Ruchika CZ, Péli ER (2020) Effect of salicylic acid pre-treatment after long-term desiccation in the moss Syntrichia ruralis (Hedw.) Web. and Mohr. Plants 9:1097
Sakakibara K, Nishiyama T, Sumikawa N, Kofuji R, Murata T, Hasebe M (2003) Involvement of auxin and homeodomain-leucine zipper I gene in rhizoid development of the moss Physcomitrella patens. Development 130:4835–4846
Sakata Y, Komatsu K, Taji T, Tanaka S (2009) Role of PP2C-mediated ABA signaling in the moss Physcomitrella patens. Plant Signal Behav 4:887–889
Sakata Y, Nakamura I, Taji T, Tanaka S, Quatrano RS (2010) Regulation of the ABA-responsive Em promoter by ABI3 in the moss Physcomitrella patens. Plant Signal Behav 5:1061–1066
Sakata Y, Komatsu K, Takezawa D (2014) ABA as a universal plant hormone. In: Lüttge U, Beyschlag W, Cushman J (eds) Progress in botany. Springer, Berlin, pp 57–96
Saruhashi M, Ghosh TK, Arai K, Ishizaki Y, Hagiwara K, Komatsu K, Shiwa Y, Izumikawa K, Yoshikawa H, Umezawa T, Sakata Y, Takezawa D (2015) Plant Raf-like kinase integrates abscisic acid and hyperosmotic stress signaling upstream of SNF1-related protein kinase2. Proc Natl Acad Sci USA 112:E6388–E6396
Saunders MJ (1986) Calcium mediation of cytokinin-induced cell division. In: Trewavas AJ (ed) Molecular and cellular aspects of calcium in plant development. Springer, Boston, pp 185–192
Sawa S, Tabata R (2011) RPK2 functions in diverged CLE signaling. Plant Signal Behav 6:86–88
Scaffidi A, Waters MT, Sun YK, Skelton BW, Dixon KW, Ghisalberti EL, Flematti GR, Smith SM (2014) Strigolactone hormones and their stereoisomers signal through two related receptor proteins to induce different physiological responses in arabidopsis. Plant Physiol 165:1221–1232
Schaefer DG, Zrÿd J-P (1997) Efficient gene targeting in the moss Physcomitrella patens. Plant J 11:1195–1206
Scholz J, Brodhun F, Hornung E, Herrfurth C, Stumpe M, Beike AK, Faltin B, Frank W, Reski R, Feussner I (2012) Biosynthesis of allene oxides in Physcomitrella patens. BMC Plant Biol 12:228
Schumaker KS, Dietrich MA (1998) Hormone-induced signaling during moss development. Annu Rev Plant Physiol Plant Mol Biol 49:501–523
Senger T, Wichard T, Kunze S, Göbel C, Lerchl J, Pohnert G, Feussner I (2005) A multifunctional lipoxygenase with fatty acid hydroperoxide cleaving activity from the moss Physcomitrella patens. J Biol Chem 280:7588–7596
Shinozawa A et al (2019) SnRK2 protein kinases represent an ancient system in plants for adaptation to a terrestrial environment. Commun Biol 2:30
Spíchal L (2012) Cytokinins—recent news and views of evolutionally old molecules. Funct Plant Biol 39:267–284
Stevenson SR et al (2016) Genetic analysis of Physcomitrella patens identifies abscisic acid non-responsive, a regulator of ABA responses unique to basal land plants and required for desiccation tolerance. Plant Cell 28:1310–1327
Stumpe M, Bode J, Göbel C, Wichard T, Schaaf A, Frank W, Frank M, Reski R, Pohnert G, Feussner I (2006) Biosynthesis of C9-aldehydes in the moss Physcomitrella patens. Biochim Biophys Acta Mol Cell Biol Lipids 1761:301–312
Stumpe M, Göbel C, Faltin B, Beike AK, Hause B, Himmelsbach K, Bode J, Kramell R, Wasternack C, Frank W, Reski R, Feussner I (2010) The moss Physcomitrella patens contains cyclopentenones but no jasmonates: mutations in allene oxide cyclase lead to reduced fertility and altered sporophyte morphology. New Phytol 188:740–749
Sun L et al (2016) Functional investigation of two 1-aminocyclopropane-1-carboxylate (ACC) synthase-like genes in the moss Physcomitrella patens. Plant Cell Rep 35:817–830
Sun Y, Harpazi B, Wijerathna-Yapa A, Merilo E, de Vries J, Michaeli D, Gal M, Cuming AC, Kollist H, Mosquna A (2019) A ligand-independent origin of abscisic acid perception. Proc Natl Acad Sci 116:24892–24899
Szweykowska A, Korcz I (1972) Inhibition of cell division in a moss protonema by some cytokinin isomers. Planta 108:279–282
Szweykowska A, Dornowska E, Cybulska A, Asiek GW (1971) The cell division response to cytokinins in isolated cell cultures of the protonema of Funaria hygrometrica and its comparison with the bud induction response. Biochem Physiol Der Pflanz 162:514–525
Szweykowska A, Korcz I, Jaskiewicz-Mroczkowska B, Metelska M (1972) The effect of various cytokinins and other factors on the protonemal cell divisions and the induction of gametophores in Ceratodon purpureus. Acta Soc Bot Pol 41:401–409
Takezawa D, Watanabe N, Ghosh TK, Saruhashi M, Suzuki A, Ishiyama K, Somemiya S, Kobayashi M, Sakata Y (2015) Epoxycarotenoid-mediated synthesis of abscisic acid in Physcomitrella patens implicating conserved mechanisms for acclimation to hyperosmosis in embryophytes. New Phytol 206:209–219
Tam THY, Catarino B, Dolan L (2015) Conserved regulatory mechanism controls the development of cells with rooting functions in land plants. Proc Natl Acad Sci 112:E3959–E3968
Tao S, Estelle M (2018) Mutational studies of the Aux/IAA proteins in Physcomitrella reveal novel insights into their function. New Phytol 218:1534–1542
Thelander M, Olsson T, Ronne H (2005) Effect of the energy supply on filamentous growth and development in Physcomitrella patens. J Exp Bot 56:653–662
Thelander M, Landberg K, Sundberg E (2018) Auxin-mediated developmental control in the moss Physcomitrella patens. J Exp Bot 69:277–290
Timmerhaus G, Hanke ST, Buchta K, Rensing SA (2011) Prediction and validation of promoters involved in the abscisic acid response in Physcomitrella patens. Mol Plant 4:713–729
Tomoi T, Kawade K, Kitagawa M, Sakata Y, Tsukaya H, Fujita T (2020) Quantitative imaging reveals distinct contributions of SnRK2 and ABI3 in plasmodesmatal permeability in Physcomitrella patens. Plant Cell Physiol 61:942–956
Toshima E, Nanjo Y, Komatsu S, Abe T, Matsuura H, Takahashi K (2014) Proteomic analysis of Physcomitrella patens treated with 12-oxo-phytodienoic acid, an important oxylipin in plants. Biosci Biotechnol Biochem 78:946–953
Vandenbussche F, Fierro AC, Wiedemann G, Reski R, Van Der Straeten D (2007) Evolutionary conservation of plant gibberellin signalling pathway components. BMC Plant Biol 7:1–17
Vesty EF et al (2016) The decision to germinate is regulated by divergent molecular networks in spores and seeds. New Phytol 211:952–966
Viaene T et al (2014) Directional auxin transport mechanisms in early diverging land plants. Curr Biol 24:2786–2791
von Maltzahn KE (1959) Interaction between kinetin and indoleacetic acid in the control of bud reactivation in Splachnum ampullaceum (L.) Hedw. Nature 183:60–61
von Schwartzenberg K (2018) Hormonal regulation of development by auxin and cytokinin in moss. In: Roberts JA (ed) Annual plant reviews online, major reference works. Wiley, Chichester, pp 246–281
von Schwartzenberg K, Kruse S, Reski R, Moffatt B, Laloue M (1998) Cloning and characterization of an adenosine kinase from Physcomitrella involved in cytokinin metabolism. Plant J 13:249–257
von Schwartzenberg K, Schultze W, Kassner H (2004) The moss Physcomitrella patens releases a tetracyclic diterpene. Plant Cell Rep 22:780–786
von Schwartzenberg K, Núñez MF, Blaschke H, Dobrev PI, Novák O, Motyka V, Strnad M (2007) Cytokinins in the bryophyte Physcomitrella patens: analyses of activity, distribution, and cytokinin oxidase/dehydrogenase overexpression reveal the role of extracellular cytokinins. Plant Physiol 145:786–800
von Schwartzenberg K, Lindner AC, Gruhn N, Šimura J, Novák O, Strnad M, Gonneau M, Nogué F, Heyl A (2016) CHASE domain-containing receptors play an essential role in the cytokinin response of the moss Physcomitrella patens. J Exp Bot 67:667–679
Walker CH, Siu-Ting K, Taylor A, O’Connell MJ, Bennett T (2019) Strigolactone synthesis is ancestral in land plants, but canonical strigolactone signalling is a flowering plant innovation. BMC Biol 17:70
Wang TL, Cove DJ, Beutelmann P, Hartmann E (1980) Isopentenyladenine from mutants of the moss, Physcomitrella patens. Phytochemistry 19:1103–1105
Wang TL, Horgan R, Cove D (1981) Cytokinins from the moss Physcomitrella patens. Plant Physiol 68:735–738
Wang W, Esch JJ, Shiu SH, Agula H, Binder BM, Chang C, Patterson SE, Bleecker AB (2006) Identification of important regions for ethylene binding and signaling in the transmembrane domain of the ETR1 ethylene receptor of Arabidopsis. Plant Cell 18:3429–3442
Wang X, Kuang T, He Y (2010) Conservation between higher plants and the moss Physcomitrella patens in response to the phytohormone abscisic acid: a proteomics analysis. BMC Plant Biol 10:192
Wang C, Liu Y, Li S-S, Han G-Z (2015) Insights into the origin and evolution of the plant hormone signaling machinery. Plant Physiol 167:872–886
Wang X et al (2019) ABRE-BINDING FACTORS play a role in the feedback regulation of ABA signaling by mediating rapid ABA induction of ABA co-receptor genes. New Phytol 221:341–355
Waters MT, Gutjahr C, Bennett T, Nelson DC (2017) Strigolactone signaling and evolution. Annu Rev Plant Biol 68:291–322
Went F (1926) On growth-accelerating substances in the coleoptile of Avena sativa. Proc k Ned Akad Van Wet 30:10–19
Werner O, Ros Espín RM, Bopp M, Atzorn R (1991) Abscisic-acid-induced drought tolerance in Funaria hygrometrica Hedw. Planta 186:99–103
Whitewoods C (2020) Evolution of CLE peptide signalling. Semin Cell Dev Biol 109:12–19
Whitewoods CD et al (2018) CLAVATA was a genetic novelty for the morphological innovation of 3D growth in land plants. Curr Biol 28:2365–2376
Wichard T, Göbel C, Feussner I, Pohnert G (2005) Unprecedented lipoxygenase/hydroperoxide lyase pathways in the moss Physcomitrella patens. Angew Chem Int Ed 44:158–161
Wolf L, Rizzini L, Stracke R, Ulm R, Rensing SA (2010) The molecular and physiological responses of Physcomitrella patens to ultraviolet-B radiation. Plant Physiol 153:1123–1134
Yamagami A, Saito C, Nakazawa M, Fujioka S, Uemura T, Matsui M, Sakuta M, Shinozaki K, Osada H, Nakano A, Asami T, Nakano T (2017) Evolutionarily conserved BIL4 suppresses the degradation of brassinosteroid receptor BRI1 and regulates cell elongation. Sci Rep 7:5739
Yamaguchi YL, Ishida T, Sawa S (2016) CLE peptides and their signaling pathways in plant development. J Exp Bot 67:4813–4826
Yao J, Waters MT (2020) Perception of karrikins by plants: a continuing enigma. J Exp Bot 71:1774–1781
Yasumura Y, Crumpton-Taylor M, Fuentes S, Harberd NP (2007) Step-by-step acquisition of the gibberellin-DELLA growth-regulatory mechanism during land-plant evolution. Curr Biol 17:1225–1230
Yasumura Y, Pierik R, Fricker MD, Voesenek LACJ, Harberd NP (2012) Studies of Physcomitrella patens reveal that ethylene-mediated submergence responses arose relatively early in land-plant evolution. Plant J 72:947–959
Yasumura Y, Pierik R, Kelly S, Sakuta M, Voesenek LACJ, Harberd NP (2015) An ancestral role for CONSTITUTIVE TRIPLE RESPONSE1 proteins in both ethylene and abscisic acid signaling. Plant Physiol 169:283–298
Yevdakova NA, von Schwartzenberg K (2007) Characterisation of a prokaryote-type tRNA-isopentenyltransferase gene from the moss Physcomitrella patens. Planta 226:683–695
Yokota T, Ohnishi T, Shibata K, Asahina M, Nomura T, Fujita T, Ishizaki K, Kohchi T (2017) Occurrence of brassinosteroids in non-flowering land plants, liverwort, moss, lycophyte and fern. Phytochemistry 136:46–55
Yoneyama K, Xie X, Yoneyama K, Kisugi T, Nomura T, Nakatani Y, Akiyama K, McErlean CSP (2018) Which are the major players, canonical or non-canonical strigolactones? J Exp Bot 69:2231–2239
Zhang J et al (2020) The hornwort genome and early land plant evolution. Nat Plants 6:107
Zhao Y (2010) Auxin biosynthesis and its role in plant development. Annu Rev Plant Biol 61:49–64
Zhao M, Li Q, Chen Z, Lv Q, Bao F, Wang X, He Y (2018) Regulatory mechanism of ABA and ABI3 on vegetative development in the moss Physcomitrella patens. Int J Mol Sci 19:1–19
Zheng B, Bai Q, Wu L, Liu H, Liu Y, Xu W, Li G, Ren H, She X, Wu G (2019) EMS1 and BRI1 control separate biological processes via extracellular domain diversity and intracellular domain conservation. Nat Commun 10:4165
Zhu J-Y, Sae-Seaw J, Wang Z-Y (2013) Brassinosteroid signalling. Development 140:1615–1620
Acknowledgements
We thank Florence Charlot and Beate Hoffmann from the IJPB for providing several pictures used in this review’s figures. We also thank Catherine Rameau, Alexandre de Saint Germain and Pierre-François Perroud from the IJPB for their kind assistance with proofreading. We are grateful to Mark Tepfer (IJPB) for his kind editing of the English.
Funding
The IJPB benefits from the support of Saclay Plant Sciences-SPS (ANR-17-EUR-0007).
Author information
Authors and Affiliations
Contributions
Both authors contributed to compiling and reading the appropriate literature and to the writing of the present review paper.
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Guillory, A., Bonhomme, S. Phytohormone biosynthesis and signaling pathways of mosses. Plant Mol Biol 107, 245–277 (2021). https://doi.org/10.1007/s11103-021-01172-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11103-021-01172-6