Despite the crucial roles of phytohormones in plant development, comparison of the exact distribution profiles of different hormones within plant meristems has thus far remained scarce. Vascular ...cambium, a wide lateral meristem with an extensive developmental zonation, provides an optimal system for hormonal and genetic profiling. By taking advantage of this spatial resolution, we show here that two major phytohormones, cytokinin and auxin, display different yet partially overlapping distribution profiles across the cambium. In contrast to auxin, which has its highest concentration in the actively dividing cambial cells, cytokinins peak in the developing phloem tissue of a Populus trichocarpa stem. Gene expression patterns of cytokinin biosynthetic and signaling genes coincided with this hormonal gradient. To explore the functional significance of cytokinin signaling for cambial development, we engineered transgenic Populus tremula × tremuloides trees with an elevated cytokinin biosynthesis level. Confirming that cytokinins function as major regulators of cambial activity, these trees displayed stimulated cambial cell division activity resulting in dramatically increased (up to 80% in dry weight) production of the lignocellulosic trunk biomass. To connect the increased growth to hormonal status, we analyzed the hormone distribution and genome-wide gene expression profiles in unprecedentedly high resolution across the cambial zone. Interestingly, in addition to showing an elevated cambial cytokinin content and signaling level, the cambial auxin concentration and auxin-responsive gene expression were also increased in the transgenic trees. Our results indicate that cytokinin signaling specifies meristematic activity through a graded distribution that influences the amplitude of the cambial auxin gradient.
•Gene expression was profiled globally across the cambium in high resolution•Auxin and cytokinin display distinct distribution profiles across the cambium•Increased cytokinin content and signaling level stimulate cambial cell divisions•Elevation of cytokinin content leads to an increased cambial auxin concentration
A new report explores how two major phytohormones, cytokinin and auxin, contribute to the control of tree trunk growth. Immanen et al. show that by boosting cytokinin biosynthesis, they can both increase auxin level and stimulate lignocellulosic biomass production. Both hormones represent optimal targets for tree breeding and forest biotechnology.
Tree bark is a highly specialized array of tissues that plays important roles in plant protection and development. Bark tissues develop from two lateral meristems; the phellogen (cork cambium) ...produces the outermost stem–environment barrier called the periderm, while the vascular cambium contributes with phloem tissues. Although bark is diverse in terms of tissues, functions and species, it remains understudied at higher resolution.
We dissected the stem of silver birch (Betula pendula) into eight major tissue types, and characterized these by a combined transcriptomics and metabolomics approach. We further analyzed the varying bark types within the Betulaceae family.
The two meristems had a distinct contribution to the stem transcriptomic landscape. Furthermore, inter- and intraspecies analyses illustrated the unique molecular profile of the phellem. We identified multiple tissue-specific metabolic pathways, such as the mevalonate/betulin biosynthesis pathway, that displayed differential evolution within the Betulaceae. A detailed analysis of suberin and betulin biosynthesis pathways identified a set of underlying regulators and highlighted the important role of local, small-scale gene duplication events in the evolution of metabolic pathways.
This work reveals the transcriptome and metabolic diversity among bark tissues and provides insights to its development and evolution, as well as its biotechnological applications.
To secure a sustainable energy source for the future, we need to develop an alternative to fossil fuels. Cellulose-based biofuel production has great potential for development into a sustainable and ...renewable energy source. The thick secondary walls of xylem cells provide a natural source of cellulose. As a result of the extensive production of wood through cambial activity, massive amounts of xylem cells can be harvested from trees. How can we obtain a maximal cellulose biomass yield from these trees? Thus far, tree breeding has been very challenging because of the long generation time. Currently, new breeding possibilities are emerging through the development of high-throughput technologies in molecular genetics. What potential does our current knowledge on the regulation of cambial activity provide for the domestication of optimal bioenergy trees? We examine the hormonal and molecular regulation of wood development with the aim of identifying the key regulatory aspects. We describe traits, including stem morphology and xylem cell dimensions, that could be modified to enhance wood production. Finally, we discuss the potential of novel marker-assisted tree breeding technologies.
Although a substantial proportion of plant biomass originates from the activity of vascular cambium, the molecular basis of radial plant growth is still largely unknown. To address whether cytokinins ...are required for cambial activity, we studied cytokinin signaling across the cambial zones of 2 tree species, poplar (Populus trichocarpa) and birch (Betula pendula). We observed an expression peak for genes encoding cytokinin receptors in the dividing cambial cells. We reduced cytokinin levels endogenously by engineering transgenic poplar trees (P. tremula x tremuloides) to express a cytokinin catabolic gene, Arabidopsis CYTOKININ OXIDASE 2, under the promoter of a birch CYTOKININ RECEPTOR 1 gene. Transgenic trees showed reduced concentration of a biologically active cytokinin, correlating with impaired cytokinin responsiveness. In these trees, both apical and radial growth was compromised. However, radial growth was more affected, as illustrated by a thinner stem diameter than in WT at same height. To dissect radial from apical growth inhibition, we performed a reciprocal grafting experiment. WT scion outgrew the diameter of transgenic stock, implicating cytokinin activity as a direct determinant of radial growth. The reduced radial growth correlated with a reduced number of cambial cell layers. Moreover, expression of a cytokinin primary response gene was dramatically reduced in the thin-stemmed transgenic trees. Thus, a reduced level of cytokinin signaling is the primary basis for the impaired cambial growth observed. Together, our results show that cytokinins are major hormonal regulators required for cambial development.
Through the diversity of cytokinin regulated processes, this phytohormone has a profound impact on plant growth and development. Cytokinin signaling is involved in the control of apical and lateral ...meristem activity, branching pattern of the shoot, and leaf senescence. These processes influence several traits, including the stem diameter, shoot architecture, and perennial life cycle, which define the development of woody plants. To facilitate research about the role of cytokinin in regulation of woody plant development, we have identified genes associated with cytokinin signaling and homeostasis pathways from two hardwood tree species.
Taking advantage of the sequenced black cottonwood (Populus trichocarpa) and peach (Prunus persica) genomes, we have compiled a comprehensive list of genes involved in these pathways. We identified genes belonging to the six families of cytokinin oxidases (CKXs), isopentenyl transferases (IPTs), LONELY GUY genes (LOGs), two-component receptors, histidine containing phosphotransmitters (HPts), and response regulators (RRs). All together 85 Populus and 45 Prunus genes were identified, and compared to their Arabidopsis orthologs through phylogenetic analyses.
In general, when compared to Arabidopsis, differences in gene family structure were often seen in only one of the two tree species. However, one class of genes associated with cytokinin signal transduction, the CKI1-like family of two-component histidine kinases, was larger in both Populus and Prunus than in Arabidopsis.
Celotno besedilo
Dostopno za:
DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
Higher plant vasculature is characterized by two distinct developmental phases. Initially, a well-defined radial primary pattern is established. In eudicots, this is followed by secondary growth, ...which involves development of the cambium and is required for efficient water and nutrient transport and wood formation. Regulation of secondary growth involves several phytohormones, and cytokinins have been implicated as key players, particularly in the activation of cell proliferation, but the molecular mechanisms mediating this hormonal control remain unknown. Here we show that the genes encoding the transcription factor AINTEGUMENTA (ANT) and the D-type cyclin CYCD3;1 are expressed in the vascular cambium of Arabidopsis roots, respond to cytokinins and are both required for proper root secondary thickening. Cytokinin regulation of ANT and CYCD3 also occurs during secondary thickening of poplar stems, suggesting this represents a conserved regulatory mechanism.
Quantitative and qualitative lignin analyses were carried out on material from the trunks of silver birch (Betula pendula Roth) trees. Two types of material were analyzed. First, whole birch trunk ...pieces were cryosectioned into cork cambium, non-conductive phloem, the cambial zone (conductive phloem, cambium and differentiating xylem), lignified xylem and the previous year's xylem; material that would show differences in lignin amount and quality. Second, clonal material from one natural birch population was analyzed to show variations between individuals and between the lignin analysis methods. The different tissues showed marked differences in lignin amount and the syringyl:guaiacyl (S/G) ratio. In the non-conductive phloem tissue containing sclereids, the S/G ratio was very low, and typical for phloem fibers and in the newly-formed xylem, as well as in the previous year's xylem, the ratio lay between five and seven, typical for broadleaf tree xylem. Clonal material consisting of 88 stems was used to calculate the S/G ratios from the thioacidolysis and CuO methods, which correlated positively with an R² value of 0.43. Comparisons of the methods indicate clearly that the CuO method is a good alternative to study the monomeric composition and S/G ratio of wood lignins.
Desorption atmospheric pressure photoionization (DAPPI) is an ambient mass spectrometry (MS) technique that allows the analysis of both polar and nonpolar compounds directly from the surfaces of ...various sample types. Here, DAPPI was used to study the chemical profiles in different parts of birch and alder tree barks. Four distinct fractions of
Betula pendula
(silver birch) bark were collected from three different developmental stages of the stem, after which the chemical profiles of the different tissue types were measured. Of special interest were triterpenoids, a class of important defensive substances, which are found in the bark of the silver birch. Additionally, the chemical profiles of lenticels and the surrounding surfaces in the phellem of
B
.
pendula
(silver birch),
Alnus glutinosa
(black alder), and
Alnus incana
(gray alder) were screened with DAPPI. Another ambient MS technique, laser ablation atmospheric pressure photoionization (LAAPPI), was further used for the mass spectrometry imaging of lenticels on the
B
.
pendula
phellem. All the studied birch bark fractions showed individual chemical profiles in DAPPI. The mass spectra from the young apical stem and the transition zone resembled each other more than the mature stem. Instead, the phellem was found to contain a high amount of triterpenoids in all the developmental stages of the stem. The most intense peaks in the DAPPI mass spectra of the birch bark fractions were those of betulin and lupeol. Betulinic and betulonic acid peaks were intense as well, and these compounds were detected especially in the lenticels of the tree samples.
Graphical abstract
Polyploidy, or genome doubling, has occurred repeatedly through plant evolution. While polyploid plants are used extensively in agriculture and horticulture, they have so far found limited use in ...forestry. Here we review the potentials of polyploid trees under climate change, and investigate if there is support for increased use. We find that polyploid trees like other plants have consistent increases in cell sizes compared to diploids, and that leaf-area based rates of photosynthesis tend to increase with increasing levels of ploidy. While no particular trend could be discerned in terms of biomass between trees of different ploidy levels, physiology is affected by polyploidization and several studies point towards a high potential for polyploid trees to adapt to drought stress. The ploidy level of most tree species is unknown, and analysis of geographical patterns in frequencies of polyploid trees are inconclusive. Artificial polyploid trees are often created by colchicine and in a few cases these have been successfully applied in forestry, but the effects of induced polyploidization in many economically important tree species remains untested. Polyploids would also be increasingly useful in tree breeding programs, to create synthetic hybrids or sterile triploids that could control unwanted spreading of germplasm in nature. In conclusion, this review suggests that polyploid trees may be superior under climate change in some cases, but that the potential of polyploids is not yet fully known and should be evaluated on a case-to-case basis for different tree species.
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•We reviewed contemporary literature on polyploid trees.•Although polyploidy is common, the ploidy level of many tree species is unknown.•Polyploidy alters anatomy, physiology and growth of trees, making some more stress tolerant.•Increased use of polyploid trees could be advantageous under climate change conditions.•Polyploids should be further investigated for their potential to increase productivity in forestry.
Due to their long lifespan, trees and bushes develop higher order of branches in a perennial manner. In contrast to a tall tree, with a clearly defined main stem and branching order, a bush is ...shorter and has a less apparent main stem and branching pattern. To address the developmental basis of these two forms, we studied several naturally occurring architectural variants in silver birch (
Betula pendula
). Using a candidate gene approach, we identified a bushy
kanttarelli
variant with a loss-of-function mutation in the
BpMAX1
gene required for strigolactone (SL) biosynthesis. While
kanttarelli
is shorter than the wild type (WT), it has the same number of primary branches, whereas the number of secondary branches is increased, contributing to its bush-like phenotype. To confirm that the identified mutation was responsible for the phenotype, we phenocopied
kanttarelli
in transgenic
BpMAX1::RNAi
birch lines. SL profiling confirmed that both
kanttarelli
and the transgenic lines produced very limited amounts of SL. Interestingly, the auxin (IAA) distribution along the main stem differed between WT and
BpMAX1::RNAi
. In the WT, the auxin concentration formed a gradient, being higher in the uppermost internodes and decreasing toward the basal part of the stem, whereas in the transgenic line, this gradient was not observed. Through modeling, we showed that the different IAA distribution patterns may result from the difference in the number of higher-order branches and plant height. Future studies will determine whether the IAA gradient itself regulates aspects of plant architecture.
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