Indian Journal of Biotechnology Vol 2, 1anuary 2003, pp 9-16
Hormonal Regulation of Moss Protonema Development and the Possible Origin of Plant Hormonal Responses in Bryophytes M M Johri* and Jacinta S D'Souza Department of Biological Sciences, Tata Institute of Fundamental Research, Homi Bhabha Road, Mumbai 400 005, India The protonema of mosses is a far simpler paradigm to understand the mechanism of hormonal action and tolerance to abiotic stresses in plants. Its developmental biology, responses to hormones and the similarity of signaling mechanisms with higher plants are reviewed. There is strong evidence for second messenger role of calcium ions in the action of cytokinin. Multiple calcium-dependent protein kinases (CDPKs) are present in the protonema. The Funaria hygrometrica CDPK gene (FhCDPK) shows the characteristic catalytic and autoinhibitory domains, the four EF hands and the highest homology to CDPKs from higher plants but far lower to liverwort or other moss CDPK genes. A 38 kDa myelin basic protein kinase (MBP kinase) is activated within minutes by abscisic acid (ABA) and salinity. As ABA also confers tolerance against desiccation and freezing and the wheat ABA-inducible promoter is fully functional in mosses, the ABA signaling mechanism seems to be highly conserved. In plants, the CDPKs are involved not only in hormonal signaling but also in the acclimation response against abiotic stresses. The manipulation of signal transduction components such as transcription factors, CDPKs and calcineurin have emerged as viable strategies to genetically engineer the stress tolerant plants. There is increasing evidence to support the origin of plant hormonal responses at the level of bryophytes. Keywords
: Funaria hygrometrica, hormonal responses
CDPKs, MBP kinase, abscisic acid, auxin, calcium, origin of
Introduction The overall development in plants is regulated by environmental and internal factors. How plants perceive various signals, transduce them and ultimately alter the growth in terms of temporal .and spatial patterns, is beginning to be comprehended. The bryophytes represent the earliest group of land plants where the phytohormone-mediated morphogenetic responses comparable to that in higher plants have been found (Bopp, 1990; Johri, 1990). The protonema of mosses such as Funaria hygrometrica Hedw. and Physcomitrella patens (Hedw.) B.S.G. have been used to study the hormonal regulation of development (Bopp & Atzorn, 1992; Cove & Knight,
* Author for correspondence: Tel: 022-22152971 Ext-2255 ; Fax: 022-22152110 E-mail: [email protected]
Abbreviations: A23187: calcium ionophore; ABA: abscisic acid; CaM: calmodulin; CCaMK: calcium regulated calmodulin-dependent PK; CDPK: calcium-dependent protein kinase; CTC: chlorotetracycline; DHP: I A-dihydropyridine; FhCDPK: Funaria hygrometrica CDPK gene; LEA: late embryogenesis abundant; MAPKKK: mitogen activated protein kinase kinase kinase; MBP kinase: myelin basic protein kinase; PCIB: p-chlorophenoxyisobutyric acid; PK: Protein kinase; SAPK: stress activated PK; SIMK: salt stress-induced MAPK.
1993; Johri, 1978). The hormonal responses are rapid and discernible either in single cells or in a group of a few cells and are thus more or less cell autonomous. This review focusses on the hormonal regulation of protonema development, the diversity of protein kinases (PKs) from the moss, F. hygrometrica and the importance of PKs in relation to abiotic stress tolerance in plants. The possible origin of hormonal responses is also discussed. Hormonal Regulation of Cell differentiation in Moss Suspension Cultures A remarkable feature of the protonemal suspension cultures of Funaria has been the long-term stability of the cell line J-2 which has now been maintained for over 32 years by repeated subculture in a low-calcium medium. During this long time, it has neither lost the potential to differentiate nor the responsiveness to phytohormones (Johri, 1974). The caulonema differentiation is regulated by inoculum size, auxin concentration and nutrient level. It marks a major developmental switch, which is turned on by biologically active auxins and ethyl ester of IAA but not by indoleacrylic acid or 2,4-dichlorophenoxyacetic acid (Johri & Desai, 1973; Johri & D'Souza, 1990). There is
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an increase In endogenous auxin during caulonema formation (Atzorn et al, 1989a, 1989b). The cytokinins induce the formation of bud initials, which arise as side branches from caulonemal cells (Gorton & Eakin, 1957). Cytokinin-over-producing mutants of P. patens form the buds constitutively (Ashton et al, 1979). ABA inhibits the growth and cytokinin-induced bud formation (Valdon & Mummery, 1971). ABAtreatment of protonemal cells is reported to increase tolerance against freezing and to confer adaptation to drought (Nagao et al, 2001; Werner et al, 1993). The endogenous level of ABA increases in moss plants under arid conditions (Bopp & Werner, 1993) and an application of ABA causes closure of stomata in the Funaria sporophyte (Garner & Paolillo, 1973). In the presence of ABA, the side branches on the protonema remain short and develop into resting structures referred to as the brood cells (Johri, 1988). Formation of new polypeptides which share epitopes with the higher plant LEA (late embryogenesis abundant) proteins, have been demonstrated in the protonema (Ainapure, 1998). The ABA- and osmotic stressinducible promoter elements from the wheat Em gene are fully functional in the moss P. patens (Knight et al, 1995). Thus, stress responses seem to be well conserved between higher plants and mosses.
Auxin-transport and -binding Sites are Involved in Auxin Response Similar to the other auxin-induced responses, the bulk medium pH changes from an initial value of about 5 to 6.5 during IAA response. In the absence of auxin, the caulonema can differentiate, but after a lag of 6 days, if the medium is buffered in the range of pH 5 - 5.5. The responsiveness of cells to auxin is also modulated by medium pH and nutrient level (Johri & D'Souza, 1990). The lag is prolonged by the auxin antagonist p-chlorophenoxyisobutyric acid (PCIB) which reduces polar, basipetal transport in Funaria rhizoids (Rose & Bopp, 1983) and is also known to compete with IAA for auxin-binding sites ( Jacobs & Hertel, 1978). In the PCIB-treated cultures, there is no inhibition of growth and in fact there is a profuse stimulation of secondary chloronema formation. Thus, both basipetal transport and IAA-binding sites seem to be involved during caulonema differentiation and chloronema inhibition. Most recently, the initial events in embryo development in Fucus distichus, a brown alga, have also been found to be linked to auxin and auxin transport (Basu et al, 2002).
The Role of Calcium in Mosses The role of calcium in cytokinin induced bud formation in Funaria and Physcomitrella is welldocumented (Schumaker & Dietrich, 1997). Using the lipophilic fluorescent calcium chelating probe-chlorotetracycline (CTC), a calcium rise following cytokinin treatment was localised to the presumptive initial cell site (Saunders & Hepler, 1981). Measurements of calcium currents using vibrating microelectrodes along a caulonema filament have shown that cytokinin application leads to an increase in the magnitude of the inward current and causes a change in the spatial properties of the current (Saunders, 1986). In a caulonemal cell maximum inward current is observed near the nucleus but after cytokinin application, there is a decrease in the current near the centre which is followed by a rise in the apical end. This rise in the inward current predicts the location of the initial cell and falls to resting levels with the onset of the initial cell outgrowth. This current can be blocked by gadolinium, which competitively inhibits calcium transport. The calcium channel blockers, verapamil and D-600 prevent the cytokinin induced bud formation and the reversal of this effect by the calcium ionophore A23l87 shows that the calcium rise is essential for bud induction. The application of A23187 in fact leads to bud formation in the absence of cytokinin (Saunders & Hepler, 1982). Inhibition of bud formation by antagonists of l,4-dihydropyridine (DHP) and the ability of DHP agonists to substitute for the presence of cytokinin shows that DHP sensitive voltage dependent calcium channels play an important role in the cytokinin response (Conrad & Hepler, 1988). G-proteins have been suggested to regulate these DHP sensitive calcium channels in Physcomitrella (Schumaker & Gizinski, 1996). There is a rise in intracellular calcium concentration in Physcomitrella in response to physical stimuli such as cold shock and touch (Russell et al, 1996). Thus, similar calcium-sensing mechanisms seem to exist in mosses and higher plants. As CDPKs are the most predominant among the downstream targets of calcium in plants, the regulation of calcium regulated kinases from Funaria has emerged as the major thrust area.
Protein Kinases from Chloronema Cells So far, at least five CDPKs and one calciumregulated CaM dependent PK (CCaMK) have been characterised from chloronema cells. A calcium-
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independent 38 kDa MBP kinase regulated by ABA is also present. The calcium is required for the autophosphorylation as well as substrate phosphorylation by the CDPKs of Mr 44,48,63 and 70 kDa (D'Souza & Johri, 1999). There is an enhancement in the autophosphorylation of 44 kDa COPK in the presence of auxin or under other physiological conditions, which also lead to caulonema differentiation in auxin-free medium. Thus, this PK could have a role in caulonema formation. This PK is recognised by moss anti-calmodulin antibodies and is also competed by the purified moss CaM during immunoprecipitation showing that it has calmodulinlike domain. The FhCDPK gene encodes a transcript of about 2.6 kb which is upregulated by nutritional deprivation. The genomic clone shows the canonical autoinhibitory region and the four EF hands (Mitra & Johri, 2000). The deduced amino acid sequence shows extensive homology with other CDPKs namely, 73% identity with the Fragaria CDPK and 71 % homology with COPK isoform-7 of Arabidopsis. The homology to the liverwort Marchantia or the moss Tortula COPKs was lower (59-64%). The codon usage in another moss Physcomitrella is also similar to higher plants (Reski et al, 1998). Plants being monophyletic in origin, the similarity of codon usage between Funaria and Arabidopsis CDPK genes could reflect either convergent evolution since the acquisition of CDPK genes by these groups of plants or a lack of divergence of the codons. The 70 kOa moss CCaMK belongs to another very important class of the calcium-regulated PKs that have a kinase domain followed by a CaM-binding domain homologous to neural visinin-like molecules (Harmon et al, 2000; Patil et al, 1995). The purified moss 70 kDa PK prefers lysine-rich histone as substrate and is fully active in the presence of 50 ~M free calcium (D'Souza & Johri, 2002b). The enzyme is completely inactive at sub-optimal levels of free calcium (23 ~M), but is activated by nanomolar levels of the moss CaM (5-100 nM). At higher CaM levels (100-1000 nM, optimum 400 nM), the autophosphorylation of the enzyme was also greatly stimulated which in turn led to an enhanced substrate phosphorylation. The activity of the moss CCaMK is thus CaM-dependent at low levels of calcium, a response which is likely to have a physiological significance. At high calcium levels which are nonphysiological, the moss enzyme becomes
independent of CaM and this response could be a part of the calcium homeostasis mechanism. The properties of the moss CCaMK are similar to lily and tobacco CCaMKs. The specific role of moss enzyme is yet to be understood. Activation of a 38 kDa MBP Kinase by ABA As mentioned earlier, a 38 kDa MBP kinase is activated in chloronema cells within minutes of ABA treatment (D'Souza & Johri, 2002a). The activation is transient, independent of calcium, specific to ABA among phytohormones and is also evoked by salt stress but not by other abiotic stresses. Salts and other compounds such as sugars, which change the intracellular water potential in the moss protonema, also activate it (Unpublished data of 0' Souza & Johri). The effects of ABA and NaCI are additive and both must be perceived independently and the signals converge at the level of MBP kinase. The moss MBP kinase seems to be similar to the stress activated PKs (SAPK) or other osmotically-activated PKs. The latter belong to the category of MAPKs such as the SIMK which is a salt-stress and pathogen induced MAPK recently described from Medicago sativa (Cardinale et al, 2002). Since ABA is also involved in conferring resistance against anhydrobiosis in moss, the overlapping activation of MBP kinase by salt and ABA seems to be a part of signalling network. The rapidity of the ABA response in Funaria indicates that as a survival strategy different from that of animals, the plant cells seem to be in a state of readiness capable of mounting a rapid initial response. After the initial response, the cells seem to synthesize new signaling proteins and other protective compounds. There is strong evidence for the ABAinducibility of the proteins sharing epitopes with the alpha subunits of the heterotrimeric G-proteins in moss F. hygrometrica (Panigrahi, 1998). Manipulation of Calcium/CaM-dependent Protein Kinases and Phosphatases to Confer Stress Tolerance in Plants The ABA and abiotic stress signaling pathways are networked in such a way that several key elements such as MAPKs, and CDPKs seem to be shared. Therefore, by manipulating the signal transduction components or pathways, it should be possible to confer or improve the stress tolerance in plants (Grover et al, 1999; Xing & Jordan, 2000). Monroy et al (1993) demonstrated a role of calcium in the
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regulation of cold acclimation-specific genes in Medicago sativa. The COPKs have been found to be one of the positive regulators of tolerance to salt and cold stresses in several plants. Maize mesophyll protoplasts expressing the GFP reporter gene driven by an ABA-inducible HVAI promoter from barley show an enhanced expression in response to ABA, salt and cold stresses and darkness. On co-transfecting these protoplasts with constitutively active forms of the Arabidopsis COPKI and COPKla, the GFP expression was found even in the absence of stress signals or ABA. Thus, activated COPKs bypass the requirement of the signals in evoking the stress signaling (Sheen, 1996). The over-expression of rice cold- and salt-inducible OsCOPK7, conferred tolerance against both the stresses in transgenic rice (Saijo et al, 2000). The COPKs have also been found to be involved in the defense response against the fungus Cladosporium fulvum in resistant tobacco (Romeis et al, 2000); mechanical strain and dehydration stress in mung bean and Arabidopsis respectively (Botella et al, 1996; Urao et al, 1994). Among other protein kinases, an Arabidopsis homologue of GSK3/shaggy-like kinase, AtGSK1, is involved in salt stress responses (Piao et al, 2001). The transgenic plants over-expressing AtGSKI showed enhanced tolerance to salinity and the NaCI responsive genes were induced in the absence of salt. There is also evidence for the involvement of other proteins such as calciumlCaM-dependent phosphatases--the calcineurin, in the stress tolerance. The expression of AtCBLl (Arabidopsis thaliana calcineurin B-like protein) is induced by stresses such as cold, drought and wounding (Kudla et al, 1999). Another gene with considerable homology to calcineurin B, is the salt overly sensitive 3 (SOS3) gene of Arabidopsis. It has been found to mediate calcium signaling associated with the acquisition of cold tolerance (Liu and Zhu, 1997). SOS3 interacts with a serine threonine kinase, the SOS2 and upon increase in cytosolic calcium in response to high salt stress, the activated SOS2/S0S3 complex seems to modify the Na+ and K+ transporters thereby causing salt tolerance (Halfter et al, 2000). Likewise, the transgenic tobacco plants coexpressing the catalytic and regulatory subunits of yeast calcineurin showed an enhanced tolerance to salt stress (Pardo et al, 1998). The above account shows understanding of the signaling
that a deeper mechanisms and
especially the role calciumlCaM dependent protein kinases and phosphatases, enables one to devise novel and viable strategies for engineering tolerance against stresses. As the protein kinases such as COPKs operate early in the signaling pathway, their manipulation also makes it possible to regulate the activity of several genes that function downstream.
Origin of Hormonal Response in Plants Distribution of Phytohormones and their Main Role The major groups of phytohormones are more or less ubiquitously distributed in plants. Auxin, cytokinin, ethylene, gibberellins and ABA have been reported from algae (Jacobs, 1986; Johri, 1990), but the evidence for their hormonal role is not unequivocal. It is only in the bryophytes that besides the presence, specific responses to above hormones have been demonstrated. The evidence for the presence and for specific effects of gibberellins in bryophytes is however, not very strong. The regulatory role of gibberellins as antheridiogens is well documented in some of the ferns of the family Schizaeaceae (Bopp, 1990; Johri, 1990). The basic responses of auxin, cytokinin, ABA and ethylene are remarkably conserved in plants. The role of auxin in caulonema differentiation has already been mentioned. Caulonema is similar to the rhizoids and both represent the same cell type, which is the forerunner of root system of tracheophytes (vascular plants). Likewise, the cytokinin-induced bud initial cell, which develops into a three-sided apical cell forming the moss gametophore, is analogous to the initial cell or a founder cell of a multicellular apical meristem. Thus, auxin and cytokinin evoke respectively the rhizogenic and shoot bud-forming responses in plants. Similar to the higher plants, ABA also arrests development and confers tolerance against water stress in mosses and at the biochemical level at least the action mechanism of ABA action seems' to be highly conserved. Ethylene is produced by axenic cultures of several species of algae, liverworts, mosses and ferns and in general retards cell division but promotes cell elongation (Johri, 1990). It suppresses the ventral row of leaves in the leafy liverwort, Plagiochila arctica (Basile & Basile, 1983). The elongation of seta in the sporophyte of the thallose liverwort Pellia epiphylla involves a dual regulation by auxin and ethylene. The elongating setae contain adequate endogenous auxin and at the same time can also respond to exogenous auxin.
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Elongating setae release more ethylene than those not undergoing elongation (Thomas et al, 1983), a feature characteristic of auxin-rich tissues undergoing cell elongation. Auxin application also enhances ethylene production in P. arctica (Law et al, 1985). In the moss F. hygrometrica, the formation of tnema cells in old cultures seems to be related to ethylene production (Rohwer & Bopp, 1985). Ethylene has also been found to promote megasporangium formation in the lycopod Selaginella wallacei presumably by blocking the final cell division of the sporogenous tissue cells (Brooks, 1973). Similar to its effects in some of the aquatic higher plants, ethylene application stimulates the elongation of frond rachis in the semi-aquatic fern Regnellidium diphyllum (Walters & Osborne, 1979). There is thus overwhelming evidence for the remarkably conserved ethylene effects between cryptogams and angiosperms and an interaction with auxin seems to be involved in many cases. Possible Acquisition of Hormonal Function by Secondary Metabolites Growth substances acting as phytohormones are also present in several bacteria and fungi as products of secondary metabolism and the notion of a metabolite acquiring a signaling or a hormonal function has received some attention. Some of the sex hormones (sexual pheromones) of algae and fungi have been characterised chemically (Kochert, 1978; AI-Hasani & Jaenicke, 1992) and chemical signaling through pheromones had already evolved in the sexual reproduction and somatic cell repair in algae (Waaland, 1986). According to Kochert (1978), the pheromones of unicellular eucarionts could be the ancestors of hormones for all multicellular eucarionts. The action of secondary metabolites (present in ancestral forms) as hormones could have acquired a regulatory role with the evolution of multicellular orgamsms.
Origin of Specific Receptors Following Kochert's general idea about the possible origin of hormones from pheromones, Schraudolf (1985, 1986) has compared the similarities between the pheromone system of Schizaeaceae and the gibberellin responses in seed plants. According to him, "the reaction of antheridiogens in Schizaeaceous ferns represents the 'moment of becoming a hormone' for gibberellin like molecules in phanerogams"
(Schraudolf, 1985). He further argues that "In contrast to animal evolution, the phylogeny of plants seems to be characterized by a post-evolution of hormonereceptor molecule. This event was a prerequisite for a common and ubiquitously distributed metabolic product to take over the function of a regulatory molecule. The phylogeny of phytohormones therefore has to be written as a phylogeny of their receptors" (Schraudolf, 1985). Following the same argument, we wish to propose that it is not difficult to visualise the origin of specific receptors or the high-affinity perception mechanisms at the level of the ancestor of land plants and the consequent acquisition of hormonal role by auxin, cytokinin, ABA, ethylene and gibberellins. In Arabidopsis the receptors for ethylene and cytokinin have been identified to be the sensory hybrid-type histidine kinase and the twocomponent systems are involved in the signal transduction (Hwang & Sheen, 2001; Urao et al, 2000). The ethylene receptor acts upstream of a Raf protein kinase (a mitogen activated protein kinase kinase kinase or MAPKKK), and the overall signaling pathway is similar to the osmoregulation pathway in yeast. The two-component histidine receptors seems to have been derived from the cyanobacterial genome as a result of horizontal transfer of genes during the origin of the ancestor of plants (Meyerowitz, 2002; Urao et al, 2000). The receptors for the other hormones have yet to be identified. As bryophytes represent the earliest group of land plants with hormonal responses, we expect the histidine protein kinase receptors to be present in them and clones homologous with ethylene receptor have been reported from P. patens (Fujiwara & Tohe, 2001). The auxin transport and biosynthesis mechanisms in the protonema of Funaria are comparable to higher plants and are thus highly conserved (Rose & Bopp, 1983; Jayaswal & Johri, 1985). Many Signaling Components could have Evolved at the Level of Common Ancestor All land plants, the embryophytes, are believed to have a monophyletic origin. Based on the comparative morphology and molecular phylogeny, the liverworts are believed to be basal and distinct. and either mosses or hornworts represent a living sister group to vascular plants (Kendric & Crane 1997). Among the most recent studies, the analysis of the mitochondrial nadl gene by Hashimoto & Sato (2001) suggests the monophyly of mosses and
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tracheophytes and the paraphyly of liverworts to these two taxa. It has been proposed that during the transition from an aqueous to the gaseous medium, the important metabolic pathways including the plant hormones in tracheophytes (vascular plants) arose from the pre-existing elements of primary metabolism in charophycean algae and bryophytes. Due to lack of information, it is difficult to comment about the presence of pre-existing elements of hormonal mechanisms in charophycean algae, but as already discussed, there is now unequivocal evidence for the origin of ethylene and cytokinin receptors from histidine kinase of blue green algae. As already mentioned, the auxin transport and biosynthetic pathways seem to be conserved in moss and higher plants; it is plausible that the similarities extend beyond this to the level of signaling components and transduction mechanisms involving calcium! calmodulin, CDPKs and MAP kinases. Interestingly, the presence of similar hormonal mechanisms in the mosses and seed plants, the two plant groups that had evolved and diverged half a billion years ago, suggests that the modules were possibly present in the presumed unicellular common ancestor of plants. As similar signaling mechanisms are utilized in the animals also, the signaling elements or components of signal transduction must have evolved and been present before the separation of plant and animal lineages. For instance the calcium signaling including CaM operates both in plants and animals. The CDPKs on the other hand, are specific to plants and must have evolved later in the ancestor of plants only. Besides plants, sequences coding for LEA proteins are also present in the genomes of micro-organisms and nematode and could have originated in the ancient cell types as a common strategy against anhydrobiosis (Browne et al, 2002). The available evidence thus suggests that the receptors and signaling elements in the extant plants had their origin from the elements in the microbial and other ancient organisms. These elements are now regulated by the eukaryotic promoters and have been shuffled around to generate different cascades. As pointed out by Schraudolf (1985), the crux of the issue in phytohormonal responses is the problem of the origin of specific receptors. With rapid advances in molecular phylogeny hormonal signaling pathways, it may become possible to trace the events that ultimately culminated in the origin of hormonal perception and signal transduction mechanisms in plants.
Conclusions The moss protonema has emerged as an excellent developmental system to study the signaling mechanisms during hormonal action and responses to abiotic stresses. The overall hormonal regulation of cell differentiation involves several interacting factors--both inhibitory and the promo tory ones. The side branch initial on a caulonema filament is pluripotent and depending on the phytohormone applied it can differentiate either into a chloronemal, a caulonemal or a bud initial cell. The role of a particular hormone can thus be visualized in channeling or fixing the terminal destiny of a progeny cell to a specific developmental fate by inhibiting the others. The available information suggests that the specific responses to hormones such as auxin, cytokinin and ABA could have evolved early at the level of bryophytes and even in these cryptogams the level of overall mechanism of their action seems comparable to that of the higher plants. Based on similar basipetal polar transport and auxin effects Hertel (1983), had visualised the importance of mosses to understand the origin, differentiation and diversification of transport and action of plant growth substances. The stage seems to be set towards a fuller realisation of this idea. The partial sequence of Funaria calcium-dependent PK gene shows extensive homology with CDPK genes isolated from higher plants. Reski et al (1998) had also observed a high degree of conservation between moss and seed plant sequences and the codon usage in moss P. patens is very similar to that of the dicotyledenous plants. We need to learn more about the identity of other signaling molecules in plants. The analysis of protein kinase genes in the genome of mosses is likely to provide additional and new information about the origin and diversification of histidine kinase type of receptors. With the demonstration of highly efficient homologous recombination in P. patens (Schaefer & Zryd, 1997), a far more rapid progress can be expected in future.
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