The mechanism of cell division has undergone significant alterations during the evolution from aquatic streptophyte algae to land plants. Two new structures evolved, the cytokinetic phragmoplast and ...the preprophase band (PPB) of microtubules, whereas the ancestral mechanism of cleavage and the centrosomes disappeared. We map cell biological data onto the recently emerged phylogenetic tree of streptophytes. The tree suggests that, after the establishment of the phragmoplast mechanism, several groups independently lost their centrosomes. Surprisingly, the phragmoplast shows reductions in the Zygnematophyceae (the sister to land plants), many of which returned to cleavage. The PPB by contrast evolved stepwise and, most likely, originated in the algae. The phragmoplast/PPB mechanism established in this way served as a basis for the 3D development of land plants.
Recent large-scale sequencing efforts and phylogenetic analyses of green organisms held a surprise. The structurally most-refined algae, the Charales, are not the sister to land plants. Instead, several papers indicate that this is the morphologically much simpler Zygnematophyceae (e.g., Spirogyra, Closterium).
Consistent with these findings, cell division in the Zygnematophyceae shows some surprisingly land plant-like features.
Recent work has provided insight into the mechanisms underlying cell division plane control in higher plants. In addition, modifications of the canonical mechanism were described for the basal land plants Marchantia and Physcomitrella.
The Arabidopsis TGA transcription factor (TF) PERIANTHIA (PAN) regulates the formation of the floral organ primordia as revealed by the pan mutant forming an abnormal pentamerous arrangement of the ...outer three floral whorls. The Arabidopsis TGA bZIP TF family comprises 10 members, of which PAN and TGA9/10 control flower developmental processes and TGA1/2/5/6 participate in stress-responses. For the TGA1 protein it was shown that several cysteines can be redox-dependently modified. TGA proteins interact in the nucleus with land plant-specific glutaredoxins, which may alter their activities posttranslationally. Here, we investigated the DNA-binding of PAN to the AAGAAT motif under different redox-conditions. The AAGAAT motif is localized in the second intron of the floral homeotic regulator AGAMOUS (AG), which controls stamen and carpel development as well as floral determinacy. Whereas PAN protein binds to this regulatory cis-element under reducing conditions, the interaction is strongly reduced under oxidizing conditions in EMSA studies. The redox-sensitive DNA-binding is mediated via a special PAN N-terminus, which is not present in other Arabidopsis TGA TFs and comprises five cysteines. Two N-terminal PAN cysteines, Cys68 and Cys87, were shown to form a disulfide bridge and Cys340, localized in a C-terminal putative transactivation domain, can be S-glutathionylated. Comparative land plant analyses revealed that the AAGAAT motif exists in asterid and rosid plant species. TGA TFs with N-terminal extensions of variable length were identified in all analyzed seed plants. However, a PAN-like N-terminus exists only in the rosids and exclusively Brassicaceae homologs comprise four to five of the PAN N-terminal cysteines. Redox-dependent modifications of TGA cysteines are known to regulate the activity of stress-related TGA TFs. Here, we show that the N-terminal PAN cysteines participate in a redox-dependent control of the PAN interaction with a highly conserved regulatory AG cis-element, emphasizing the importance of redox-modifications in the regulation of flower developmental processes.
Celotno besedilo
Dostopno za:
DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
The colonization of land by streptophyte algae, ancestors of embryophyte plants, was a fundamental event in the history of life on earth. Bryophytes are early diversifying land plants that mark the ...transition from freshwater to terrestrial ecosystems. The amphibious liverwort
can thrive in aquatic and terrestrial environments and thus represents an ideal organism to investigate this major transition. Therefore, we aimed to establish a transformation protocol for
to make it amenable for genetic analyses. An
transformation procedure using
callus tissue allows to generate stably transformed plants within 10 weeks. Furthermore, for comprehensive studies spanning all life stages, we demonstrate that the switch from vegetative to reproductive development can be induced by both flooding and poor nutrient availability. Interestingly, a single
plant can consecutively adapt to different growth environments and forms distinctive and reversible features of the thallus, photosynthetically active tissue that is thus functionally similar to leaves of vascular plants. The morphological plasticity affecting vegetative growth, air pore formation, and rhizoid development realized by one genotype in response to two different environments makes
ideal to study the adaptive molecular mechanisms enabling the colonialization of land by aquatic plants.
Glutaredoxins (GRXs) are small oxidoreductases that are involved in various cellular processes and play a crucial role in responses to oxidative stress. Three GRX subgroups exist in plants, and GRXs ...with active sites of the CPYC and CGFS types are common to pro- and eukaryotes. In contrast, GRXs with the CC type motif have so far only been identified in land plants. Here, we report that the two CC-type GRXs ROXY1 and ROXY2 together control anther development in Arabidopsis thaliana. Single roxy1 and roxy2 mutants are fertile and produce normal anthers. However, roxy1 roxy2 double mutants are sterile and do not produce pollen. Strikingly, abaxial and adaxial anther lobe differentiation are differently affected, with early lobe differentiation being defective in the adaxial lobes, whereas later steps during pollen mother cell differentiation are disrupted in the abaxial lobes. Expression studies show that ROXY1 and ROXY2 are expressed with overlapping patterns during anther development. Lack of ROXY1 and ROXY2 function affects a large number of anther genes at the transcriptional level. Genetic and RT-PCR data imply that ROXY1/2 function downstream of the early-acting anther gene SPOROCYTELESS/NOZZLE and upstream of DYSFUNCTIONAL TAPETUM1, controlling tapetum development. Mutagenesis of a conserved glutathione-binding glycine in the ROXY1 protein indicates that CC-type GRXs need to interact with glutathione to catalyze essential biosynthetic reactions. Analysis of these two novel anther genes indicates that redox regulation, as well as participating in plant stress defense mechanisms, might play a major role in the control of male gametogenesis.
Establishment of morphological novelties has contributed to the enormous diversification of floral architecture. One such novelty, flower monosymmetry, is assumed to have evolved several times ...independently during angiosperm evolution. To date, analysis of monosymmetry regulation has focused on species from taxa where monosymmetry prevails, such as the Lamiales and Fabaceae. In Antirrhinum majus, formation of a monosymmetric corolla is specified by the activity of the TCP transcription factors CYCLOIDEA (CYC) and DICHOTOMA (DICH). It was shown that establishment of monosymmetry likely requires an early asymmetric floral expression of CYC homologs that needs to be maintained until late floral stages. To understand how CYC homologs might have been recruited during evolution to establish monosymmetry, we characterized the likely CYC ortholog IaTCP1 from Iberis amara (Brassicaceae). Species of the genus Iberis form a monosymmetric corolla, whereas the Brassicaceae are otherwise dominated by genera developing a polysymmetric corolla. Instead of four equally sized petals, I. amara produces two small adaxial and two large abaxial petals. The timing of IaTCP1 expression differs from that of its Arabidopsis homolog TCP1 and other CYC homologs. IaTCP1 lacks an asymmetric early expression but displays a very strong differential expression in the corolla at later floral stages, when the strongest unequal petal growth occurs. Analysis of occasionally occurring peloric Iberis flower variants and comparative functional studies of TCP homologs in Arabidopsis demonstrate the importance of an altered temporal IaTCP1 expression within the Brassicaceae to govern the formation of a monosymmetric corolla.
Eukaryotic life cycles alternate between haploid and diploid phases and in phylogenetically diverse unicellular eukaryotes, expression of paralogous homeodomain genes in gametes primes the ...haploid-to-diploid transition. In the unicellular chlorophyte alga
KNOX and BELL TALE-homeodomain genes mediate this transition. We demonstrate that in the liverwort
paternal (sperm) expression of three of five phylogenetically diverse BELL genes, Mp
, and maternal (egg) expression of both Mp
and Mp
mediate the haploid-to-diploid transition. Loss-of-function alleles of Mp
result in zygotic arrest, whereas a loss of either maternal or paternal Mp
results in variable zygotic and early embryonic arrest. Expression of Mp
and Mp
during diploid sporophyte development is consistent with a later role for these genes in patterning the sporophyte. These results indicate that the ancestral mechanism to activate diploid gene expression was retained in early diverging land plants and subsequently co-opted during evolution of the diploid sporophyte body.
Glutaredoxins (GRXs) are small oxidoreductases of the thioredoxin family proteins that can either regulate the thiol redox state of proteins or are linked to iron metabolism because of their ability ...to incorporate iron-sulfur 2Fe–2S clusters. Here we review recent research on a land plant-specific class of GRX-like proteins, which are characterized by the conserved CC motif in the active centre. Loss-of-function mutants of CC-type GRXs in Arabidopsis (also named ROXYs), maize, and rice have unraveled a role in floral development, including regulation of organ primordia initiation, control of organ identity gene expression, and progression into meiosis in the male germ line. Other CC-type GRXs play a role in stress responses, most likely through their capacity to regulate nuclear gene expression. Consistently, CC-type GRXs, physically and genetically interact with individual members of the TGA transcription factor family. One of the challenges in the future is to unravel whether ROXYs control the redox state of TGA factors or other yet unknown target proteins or whether they regulate gene expression through other processes. Other intriguing questions concern the original function of the first CC-type GRXs in basal land plants and their potential contribution to the extremely successful radiation of angiosperms.
Recent findings expanded our knowledge about plant redox regulation in stress responses by demonstrating that redox processes exert crucial nuclear regulatory functions in meristems and other ...developmental processes. Analyses of redox-modulated transcription factor functions and coregulatory ROXYs, CC-type land-plant specific glutaredoxins, reveal new insights into the redox control of plant transcription factors and participation of ROXYs in plant development. The role for ROS and redox signaling in response to low-oxygen conditions further strengthens the importance of redox processes in meristems and tissue differentiation as well as for adaptation to changing environments effecting food crop productivity.
Flower symmetry is considered a morphological novelty that contributed significantly to the rapid radiation of the angiosperms, which already puzzled Charles Darwin and prompted him to name this ...phenomenon an 'abominable mystery'. In 2009, the bicentenary of Darwin's birth and the 150th anniversary of the publication of his seminal work, 'On the Origin of Species', this question can now be more satisfactorily readdressed. Understanding the molecular control of monosymmetry formation in the model species Antirrhinum opened the path for comparative studies with non-model species revealing modifications of this trait. TCP transcription factors, named after TEOSINTE BRANCHED 1 in maize, CYCLOIDEA in snapdragon and PCF in rice, control flower monosymmetry development and contributed to establishing this trait several times independently in higher angiosperms. The joint advances in evolutionary and developmental plant research, combined in the novel research field named Evo/Devo, aim at elucidating the molecular mechanisms and strategies to unravel the mystery of how this diversity has been generated.
The origin of a terrestrial flora in the Ordovician required adaptation to novel biotic and abiotic stressors. Oil bodies, a synapomorphy of liverworts, accumulate secondary metabolites, but their ...function and development are poorly understood. Oil bodies of Marchantia polymorpha develop within specialized cells as one single large organelle. Here, we show that a class I homeodomain leucine-zipper (C1HDZ) transcription factor controls the differentiation of oil body cells in two different ecotypes of the liverwort M. polymorpha, a model genetic system for early divergent land plants. In flowering plants, these transcription factors primarily modulate responses to abiotic stress, including drought. However, loss-of-function alleles of the single ortholog gene, MpC1HDZ, in M. polymorpha did not exhibit phenotypes associated with abiotic stress. Rather, Mpc1hdz mutant plants were more susceptible to herbivory, and total plant extracts of the mutant exhibited reduced antibacterial activity. Transcriptomic analysis of the mutant revealed a reduction in expression of genes related to secondary metabolism that was accompanied by a specific depletion of oil body terpenoid compounds. Through time-lapse imaging, we observed that MpC1HDZ expression maxima precede oil body formation, indicating that MpC1HDZ mediates differentiation of oil body cells. Our results indicate that M. polymorpha oil bodies, and MpC1HDZ, are critical for defense against herbivory, but not for abiotic stress tolerance. Thus, C1HDZ genes were co-opted to regulate separate responses to biotic and abiotic stressors in two distinct land plant lineages.
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•Oil body cell differentiation in M. polymorpha is positively regulated by MpC1HDZ•High expression levels of MpC1HDZ precede oil body differentiation•Terpenoid-rich oil bodies protect the plant against arthropod herbivores
Most of the chemical diversity of liverworts resides within oil body cells, a synapomorphy of the lineage. Romani, Banic et al. show that oil bodies defend the plant against arthropods. Moreover, oil body cell differentiation requires the MpC1HDZ transcription factor, which shows high gene expression levels prior to oil body differentiation.
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