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Similar results were obtained using an RNA probe obtained by in vitro transcription of PrSCL1 in either the antisense or sense orientation. In situ localization of PrSCL1 and PrSHR had already been described in competent hypocotyls from day-old seedlings during adventitious rooting [ 17 ]. PrSCL2 mRNA levels increased in the absence of exogenous auxin in both rooting-competent hypocotyl cuttings from day-old seedlings and rooting-non-competent epicotyl cuttings from day-old seedlings.

The expression of two genes, PrSCL1 and PrSHR , which are associated with auxin-dependent and auxin-independent signaling pathways, respectively, in rooting-competent cuttings [ 16 ],[ 17 ] were also analyzed by in situ hybridization in non-competent cuttings. No specific tissue-localization was observed in any samples during adventitious rooting. Endogenous distribution of indoleacetic acid IAA in hypocotyl cuttings from day-old Pinus radiata seedlings. Endogenous distribution of indoleacetic acid IAA in hypocotyl and epicotyl cuttings from day-old Pinus radiata seedlings. Auxin-dependent adventitious root formation in pine is associated with a directional flow of auxin in combination with the competition of neighboring cells for free auxin [ 10 ].

Tissue-specific auxin gradients can elicit specific cellular responses. The role of the endogenous auxin distribution in rooting-competent and non-competent tissues during adventitious root formation was addressed by analyzing the indoleacetic acid IAA distribution.

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No auxin accumulation was detected in the cambial cells in non-competent hypocotyls or epicotyls. No signal was observed when tissues were hybridized in the absence of the antibody Additional file 6. Plants do not lose their developmental potentialities during differentiation and retain a certain level of plasticity [ 54 ], either by maintaining pro-embryonic or meristematic cells in the adult tissues or by a major developmental reprogramming to acquire the embryonic or meristematic status [ 55 ].

The plasticity of plant tissues results in the regenerative capacity of cells other than those of meristem, lateral root initials or zygotes. A decline in the regenerative capacity of somatically differentiated cells in an ectopic location is associated with age and maturation in forest tree species [ 13 ]. Efforts have been made to identify genes associated with plant cell fate switches [ 34 ],[ 38 ]; however, pluripotency or indeterminacy genes, with high expression levels in non-differentiated embryonic cells or at the very early stages of development, significantly reduced or even no expression levels in adult tissues that have lost their regenerative capacities, but maintained in tissues with regenerative capacities or induced after the reprogramming of adult cells during regeneration [ 56 ], have not been described.

GRAS proteins are involved in a diverse suite of physiological and developmental processes ranging from light and hormone signal transduction to organ identity and tissue differentiation [ 57 ],[ 58 ]. Additionally, they have been involved in root tip regeneration [ 59 ] and in cell reprogramming [ 38 ]. GRAS proteins have been identified as homologous proteins to the STAT proteins in animals [ 60 ], which have also been associated with differentiation, reprogramming and regeneration [ 61 ],[ 62 ].

A large gene family encodes GRAS proteins in pine. Supporting cDNAs were identified for at least 32 unique members in P.

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Eighteen members were identified in P. Pairwise sequence similarities among predicted polypeptides for each GRAS member of the different pine and spruce species confirmed that they may represent intra- or inter-specific alleles of the same genes, similar to those described for other gene families in conifer species [ 68 ],[ 69 ].

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The HAM family contains the AtSCL26 subfamily, which may be the result of a high number of duplication events for conifer sequences compared with their angiosperm counterparts. Conifers diverged from angiosperms million years ago [ 70 ]. The phylogenetic relationship between conifers and angiosperms highlights the ancient diversification of this family, which may precede the transition to terrestrial environments, as suggested by Engstrom [ 71 ] based on comparisons among GRAS proteins from angiosperms, bryophytes and lycophytes, but not gymnosperms.

The ancient diversification and the non-clustering of conifer sequences suggests functions or modes of action for these proteins in primary constitutive or induced processes [ 72 ]-[ 77 ]. An analysis of the polypeptide sequences shows a high degree of conservation in the representative GRAS core motifs Additional file 3 [ 52 ],[ 57 ],[ 58 ], which are involved in transcriptional regulation, indicating that the transcriptional regulatory machinery is also conserved in conifers.

The amino acid compositional profile of the N-terminus of GRAS proteins from pine is very similar to that of the intrinsically disordered proteins and contains an enrichment in disorder-promoting residues Additional files 4 and 5.

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However, the C-domain shows a compositional profile similar to that of fully structured proteins, as described for other GRAS proteins [ 57 ],[ 58 ]. Disordered proteins lack a well-defined three dimensional structure, resulting in an extreme structural flexibility that enables them to form highly specific complexes with different proteins or nucleic acids in a reversible and transient low-affinity interaction, depending on the changing physiological, developmental or environmental conditions [ 53 ],[ 79 ]. Intrinsic disorder has been described for several families of plant transcription factors, and intrinsically disordered proteins have been associated with key cellular and signaling processes [ 80 ]-[ 82 ].

The intrinsic disorder could be a way to increase functional diversity and the complexity of biological networks without increasing the size of the families, or even, the size of the genome, and it was proposed as the mechanism involved in the functional divergence within GRAS subfamilies [ 57 ],[ 58 ]. Despite the highly variable sequence of the N-terminus, GRAS proteins in pine show conserved disordered profiles when compared with GRAS proteins from angiosperm species of the same subfamily Additional file 5 [ 57 ],[ 58 ].

This is in agreement with previous suggestions [ 83 ],[ 84 ], indicating that the pattern of protein disorder could be more conserved through evolution than the amino acid sequence in the N-terminus. Similar results have been described for the mammalian Myc proteins [ 85 ]. Consequently, mutations that do not affect the general disorder pattern would allow the conservation of specific protein interactions and, hence, functions. The conservation of the protein motifs and structures, the absence of a particular conifer subfamily, and the intrinsically disordered N-terminal domain can account for the versatile roles of these proteins in tree biology and for the molecular mechanisms regulating their expression levels and functions.

The dynamic ability of intrinsically disordered proteins to recognize multiple molecular partners reveals the need for a synchronous spatio-temporal connection between the functionally appropriate GRAS genes and proteins participating in specific functions. Individual genes within each group may have acquired different and specialized functions, some of which may relate to competence and the reprogramming of adult cells to form adventitious roots.

At this stage, embryo polarization occurs, but tissue differentiation has not been yet completed; therefore, these tissues, along with the proliferating embryogenic masses, may be sources of non-determined or pluripotent cells associated with the establishment of tissue domains [ 47 ].

Consequently, these genes play key roles in the initial establishment of embryo tissue domains or hormone gradients [ 86 ]. These results suggest that the expression of these genes is not only restricted to embryonic development but extended to other processes. We then analyzed if the expression levels of genes associated with the early stages of embryo formation could be significantly reduced or even non-existent in cuttings that have lost their rooting capacity, but maintained in rooting-competent tissues or induced after the reprogramming of adult competent cells to form adventitious roots.

These results indicate that PrSCL6 and PrSCR , in addition to their functions in embryo development, are associated with an embryonic characteristic that could result in the competence for adventitious organogenesis in cuttings. Therefore, both genes could be associated with embryonic cells or with the very early stages of development. Their mRNA levels were significantly reduced or even lost in older and more mature rooting cuttings that had lost their rooting capacities, but were maintained in competent hypocotyls or increased after the reprogramming of adult competent cells during adventitious root formation.

This would make them candidate genes for rooting competence and cell reprogramming. The expression profiles in epicotyls could be associated with the presence of meristematic tissues in these cuttings, such as the shoot axillary meristem or cambium [ 46 ],[ 87 ]. Therefore, the participation of these genes in determining whether cells become roots in competent tissues cannot be discarded. Additionally, all these genes are expressed or induced at the very early stages of adventitious root formation before the onset of cell divisions leading to the formation of a root meristem.

The functional analysis of genes based on their subfamilies indicates a possible role in determination and patterning. SCR and SHR are involved in root meristem determination [ 43 ],[ 44 ] and, along with other transcription factors, have been involved in reprogramming in Arabidopsis [ 38 ].

Additionally, PrSCL1 , which may be related to the rooting process, has been associated with the adventitious and lateral root meristem of pine and chestnut [ 16 ],[ 46 ], and with the shoot axillary meristem in chestnut [ 46 ]. Therefore, this subfamily is also functionally diverse. Overall, a role in adventitious root competence, reprogramming and determination could be envisaged for a subset of the pine GRAS genes. In these cuttings, expression spread into the cortex and dividing cells. The asymmetrical increase in mRNA during the earliest stages of adventitious root formation in similar cell types at different developmental stages suggests the presence of specific cellular signaling pathways or specific factors in pine, perhaps distributed in cell-type- and developmental-stage-specific contexts in the tissues involved in rooting, which could be crucial for rooting capacity [ 18 ],[ 46 ].

The nature of these signaling pathways or factors is unknown. De novo organ formation and cell specification are processes involving rearrangements of tissue polarity, with the temporal and spatial distribution of auxin being a very important player, contributing to tissue polarization and patterning [ 93 ]. No differences in auxin uptake, accumulation or metabolism were found between rooting-competent and non-competent hypocotyls and epicotyls at the base of the cuttings [ 10 ]. This result indicated that rooting-competent tissues could retain an intrinsic capacity to maintain or accumulate auxin after excision, which could be crucial for rooting.

The cellular capacity of initial cells to produce auxin gradients may be a mechanism involved in the determination and maintenance of meristem, the induction of lateral primordia at the shoot meristem, and the formation of lateral roots or adventitious roots [ 20 ],[ 94 ]-[ 96 ]. Auxin distribution largely depends on the dynamic expression and subcellular localization of the PIN auxin-carrier proteins [ 97 ].

However, PIN activity can be modulated by endogenous or exogenous signals, such as other hormones, stress or tissue-specific factors, to trigger developmental decisions that could initiate regeneration by triggering cell fates or other local changes [ 37 ],[ 87 ],[ 98 ]-[ ]. No differences in the wounding stress response were observed between competent and non-competent cuttings [ ]; therefore, other tissue-dependent signals could also trigger re-patterning either by inducing cell-fate respecification or by re-establishing the auxin distribution.

Transcription factors are main players in regulatory modules controlling auxin gradients, positional information and the development of polarity fields, resulting in a cross regulatory network involved in organ formation [ ]-[ ]. Sabatini et al.


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However, the SHR pathway regulates root development through a transcriptional regulatory network and also by affecting the expression of genes involved in cytokinin and auxin signaling in Arabidopsis , resulting in the fine-tuning of hormonal responses [ 87 ],[ 99 ],[ ]. Adventitious root forming treatments induce root meristem patterning genes, such as GRAS genes, before the onset of cell division in competent cells. The same GRAS genes also may play a role during the earliest stages of embryogenesis, initial-forming and polarization.

The capacity to maintain or recruit root meristem or embryonic programs in response to a specific stimulus seems to be key in switching cells into different developmental programs, both in herbaceous and woody plants, including forest tree species [ 34 ]-[ 36 ],[ 38 ],[ ]. However, whether this pattern of expression represents a maintenance, a dedifferentiation or a transdifferentiation to an embryonic or root identity, or it represents a different adult developmental program unique to regeneration, as was described in Arabidopsis [ ], remains unknown. Pine P. Don seeds were germinated and seedlings were grown as previously described [ 16 ].

Cuttings for adventitious root induction were prepared according to [ 16 ]. Briefly, hypocotyl cuttings from day-old seedlings, including the intact epicotyl, and hypocotyl or epicotyl cuttings from day-old pine seedlings were prepared by severing the hypocotyl or epicotyl at its base, and trimming it to a length of 2. All but one apical tuft of needles were removed from the epicotyls to obtain a foliar surface similar to that of the hypocotyls.

Cuttings without IBA treatment were used as controls. IBA was obtained from Sigma St. Hypocotyls treated with DMSO were also used as controls in these experiments. Conditions for root induction were the same as described for seedling growth [ 16 ]. Embryogenic line M95, provided by Dr. The pH of the media was adjusted to 5. Solutions of amino acids and abscisic acid were filter sterilized and added to the cooled autoclaved medium.

Total RNA isolation and quantification from cuttings have been previously described [ 16 ]. RNA was also extracted from different organs of plant seedlings as specified in each experiment. RNA was prepared from at least two biological replicates.

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The conserved C-terminal region of the GRAS proteins, plus as much of the N-terminal region as the shortest protein sequence allowed, were used for the phylogenetic analysis as previously described [ 16 ],[ 17 ]. Primer design, efficiency analyses, and polymerase chain reactions were carried out as previously described [ 16 ].

Primers for amplification of P. The probes were partially hydrolyzed to an average length of nucleotides by alkali treatment. Photographs were taken with an Olympus digital camera on a Nikon microscope under bright-field illumination.


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Controls were performed by replacing the first antibody with PBS. The data sets supporting the results of this article are included within the article and its additional files. The nucleotide sequences of P. Greenwood MS: Rejuvenation of forest trees. Plant Growth Regul. Clonal Forestry: Genetics, Biotechnology and Application.