Auxin Regulation of Caulonema Formation in Moss Protonema

Johri, M. M.; Desai, Shaila

doi:10.1038/newbio245223a0

Cited by 85 publications

(63 citation statements)

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“…However, one might expect effects, i.e. reduced caulonema formation and gametophore internode elongation, opposite to those resulting from exogenous IAA application (Ashton et al, 1979;Fujita et al, 2008;Johri and Desai, 1973). Indeed, the Ppshi1 and Ppshi2 single-knockout mutants possessed these expected traits.…”

Section: Discussionmentioning

confidence: 96%

“…Auxin also functions as a hormone in bryophytes, and IAA application triggers physiological responses such as the chloronemato-caulonema transition (Johri and Desai, 1973), stem elongation (Fujita et al, 2008) and rhizoid emergence from the leafy shoot (Ashton et al, 1979). With the completion of the genome sequence of the moss Physcomitrella patens, it became clear that genes involved in auxin transport, perception and signalling in seed plants are present also in mosses (Rensing et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

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Homologues of the Arabidopsis thaliana SHI/STY/LRP1 genes control auxin biosynthesis and affect growth and development in the moss Physcomitrella patens

et al. 2010

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SUMMARYThe plant hormone auxin plays fundamental roles in vascular plants. Although exogenous auxin also stimulates developmental transitions and growth in non-vascular plants, the effects of manipulating endogenous auxin levels have thus far not been reported. Here, we have altered the levels and sites of auxin production and accumulation in the moss Physcomitrella patens by changing the expression level of homologues of the Arabidopsis SHI/STY family proteins, which are positive regulators of auxin biosynthesis genes. Constitutive expression of PpSHI1 resulted in elevated auxin levels, increased and ectopic expression of the auxin response reporter GmGH3pro:GUS, and in an increased caulonema/chloronema ratio, an effect also induced by exogenous auxin application. In addition, we observed premature ageing and necrosis in cells ectopically expressing PpSHI1. Knockout of either of the two PpSHI genes resulted in reduced auxin levels and auxin biosynthesis rates in leafy shoots, reduced internode elongation, delayed ageing, a decreased caulonema/chloronema ratio and an increased number of axillary hairs, which constitute potential auxin biosynthesis sites. Some of the identified auxin functions appear to be analogous in vascular and non-vascular plants. Furthermore, the spatiotemporal expression of the PpSHI genes and GmGH3pro:GUS strongly overlap, suggesting that local auxin biosynthesis is important for the regulation of auxin peak formation in non-vascular plants.

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Section: Discussionmentioning

confidence: 96%

Section: Introductionmentioning

confidence: 99%

Homologues of the Arabidopsis thaliana SHI/STY/LRP1 genes control auxin biosynthesis and affect growth and development in the moss Physcomitrella patens

et al. 2010

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“…We also investigated the regulation of the RSL network by auxin, a key positive regulator of root hair development in angiosperms and the chloronema-to-caulonema transition in mosses (18,(32)(33)(34). Auxin positively regulates the expression of RSL class I genes in P. patens (24) (Fig.…”

Section: Rsl Network Controls Rootmentioning

confidence: 99%

Recruitment and remodeling of an ancient gene regulatory network during land plant evolution

Pires

Breuninger

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

123

105

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The evolution of multicellular organisms was made possible by the evolution of underlying gene regulatory networks. In animals, the core of gene regulatory networks consists of kernels, stable subnetworks of transcription factors that are highly conserved in distantly related species. However, in plants it is not clear when and how kernels evolved. We show here that RSL (ROOT HAIR DEFECTIVE SIX-LIKE) transcription factors form an ancient land plant kernel controlling caulonema differentiation in the moss Physcomitrella patens and root hair development in the flowering plant Arabidopsis thaliana. Phylogenetic analyses suggest that RSL proteins evolved in aquatic charophyte algae or in early land plants, and have been conserved throughout land plant radiation. Genetic and transcriptional analyses in loss of function A. thaliana and P. patens mutants suggest that the transcriptional interactions in the RSL kernel were remodeled and became more hierarchical during the evolution of vascular plants. We predict that other gene regulatory networks that control development in derived groups of plants may have originated in the earliest land plants or in their ancestors, the Charophycean algae.T he development of multicellular organisms is controlled by gene regulatory networks (GRNs) and the reorganization of GRN architecture is thought to be a major factor underlying morphological evolution (1-5). GRNs are hierarchic and modular structures where four major component classes can be identified (3): at the periphery of GRNs are differentiation gene batteries encoding proteins that execute cell type-specific functions (such as building a pigmented cell); upstream of these batteries are switches that allow or prevent subcircuits to function in specific developmental contexts, and "plug-ins," small subcircuits that are flexibly and repeatedly used during development (such as signal transduction pathways); at the core of GRNs are kernels, small conserved subcircuits that execute specific developmental functions (such as defining spatial patterns in an embryo). Kernels are comprised of transcription factors that are highly conserved in distantly related species and are unusually stable components of GRNs.Ancient kernels that regulate body plan and organ development are highly conserved among diverse groups of metazoans (animals) (6-10). In contrast, the core components of plant GRNs are difficult to identify because of the dynamic nature of plant genome evolution and the plastic character of plant development. Floral homeotic genes form a relatively recent kernel controlling flower development (11). Homologs of KNOX and LEAFY transcription factors control shoot development in vascular plants and sporophyte development in mosses (12-15). KNOX/BEL genes also control the development of the diploid phase in unicellular chlorophytes (16) and the haploid-to-diploid transition in mosses (15), suggesting that KNOX and LEAFY genes may be core members of ancient GRNs that control diploid development in plants. Auxin signaling (17,18), et...

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“…It is a developmental switch, which is turned on only by biologically active auxins (Johri and Desai, 1973;Johri and D'Souza, 1990). Endogenous auxin has been shown to be involved in caulonema formation (Atzorn et al, 1989a;1989b).…”

Section: Auxin Regulation Of Caulonema and Protonemal Rhizoid Differementioning

confidence: 99%

Hormonal regulation in green plant lineage families

Johri

2008

Physiol Mol Biol Plants

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The patterns of phytohormones distribution, their native function and possible origin of hormonal regulation across the green plant lineages (chlorophytes, charophytes, bryophytes and tracheophytes) are discussed. The five classical phytohormonesauxins, cytokinins, gibberellins (GA), abscisic acid (ABA) and ethylene occur ubiquitously in green plants. They are produced as secondary metabolites by microorganisms. Some of the bacterial species use phytohormones to interact with the plant as a part of their colonization strategy. Phytohormone biosynthetic pathways in plants seem to be of microbial origin and furthermore, the origin of high affinity perception mechanism could have preceded the recruitment of a metabolite as a hormone. The bryophytes represent the earliest land plants which respond to the phytohormones with the exception of gibberellins. The regulation by auxin and ABA may have evolved before the separation of green algal lineage. Auxin enhances rhizoid and caulonemal differentiation while cytokinins enhance shoot bud formation in mosses. Ethylene retards cell division but seems to promote cell elongation. The presence of responses specific to cytokinins and ethylene strongly suggest the origin of their regulation in bryophytes. The hormonal role of GAs could have evolved in some of the ferns where antheridiogens (compounds related to GAs) and GAs themselves regulate the formation of antheridia.During migration of life forms to land, the tolerance to desiccation may have evolved and is now observed in some of the microorganisms, animals and plants. Besides plants, sequences coding for late embryogenesis abundant-like proteins occur in the genomes of other anhydrobiotic species of microorganisms and nematodes. ABA acts as a stress signal and increases rapidly upon desiccation or in response to some of the abiotic stresses in green plants. As the salt stress also increases ABA release in the culture medium of cyanobacterium Trichormus variabilis, the recruitment of ABA in the regulation of stress responses could have been derived from prokaryotes and present at the level of common ancestor of green plants. The overall hormonal action mechanisms in mosses are remarkably similar to that of the higher plants. As plants are thought to be monophyletic in origin, the existence of remarkably similar hormonal mechanisms in the mosses and higher plants, suggests that some of the basic elements of regulation cascade could have also evolved at the level of common ancestor of plants. The networking of various steps in a cascade or the crosstalk between different cascades is variable and reflects the dynamic interaction between a species and its specific environment.

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Auxin Regulation of Caulonema Formation in Moss Protonema

Cited by 85 publications

References 10 publications

Homologues of the Arabidopsis thaliana SHI/STY/LRP1 genes control auxin biosynthesis and affect growth and development in the moss Physcomitrella patens

Homologues of the Arabidopsis thaliana SHI/STY/LRP1 genes control auxin biosynthesis and affect growth and development in the moss Physcomitrella patens

Recruitment and remodeling of an ancient gene regulatory network during land plant evolution

Hormonal regulation in green plant lineage families

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