A Talk between Flavonoids and Hormones to Reorient the Growth of Gymnosperms.

Plants reorient the growth of affected organs in response to the loss of gravity vector. In trees, this phenomenon has received special attention due to its importance for the forestry industry of conifer species. Sustainable management is a key factor in improving wood quality. It is of paramount importance to understand the molecular and genetic mechanisms underlying wood formation, together with the hormonal and environmental factors that affect wood formation and quality. Hormones are related to the modulation of vertical growth rectification. Many studies have resulted in a model that proposes differential growth in the stem due to unequal auxin and jasmonate allocation. Furthermore, many studies have suggested that in auxin distribution, flavonoids act as molecular controllers. It is well known that flavonoids affect auxin flux, and this is a new area of study to understand the intracellular concentrations and how these compounds can control the gravitropic response. In this review, we focused on different molecular aspects related to the hormonal role in flavonoid homeostasis and what has been done in conifer trees to identify molecular players that could take part during the gravitropic response and reduce low-quality wood formation.

De novo transcriptome analysis provides insights into the salt tolerance of Podocarpus macrophyllus under salinity stress.

BACKGROUND: Soil salinization is causing ecosystem degradation and crop yield reduction worldwide, and elucidation of the mechanism of salt-tolerant plants to improve crop yield is highly significant. Podocarpus macrophyllus is an ancient gymnosperm species with a unique environmental adaptation strategy that may be attributed to its lengthy evolutionary process. The present study investigated the physiological and molecular responses of P. macrophyllus plants to salt stress by analyzing its photosynthetic system and antioxidant enzyme activity. We also analyzed the differentially expressed genes (DEGs) in P. macrophyllus under salt stress using RNA sequencing and de novo transcriptome assembly. RESULTS: Salt treatment significantly affected the photosynthetic system in P. macrophyllus seedlings, which decreased chlorophyll content, altered chloroplast ultrastructure, and reduced photosynthesis. The activities of antioxidant enzymes increased significantly following salt stress treatment. Transcriptome analysis showed that salt stress induced a large number of genes involved in multiple metabolic and biological regulation processes. The transcription levels of genes that mediate phytohormone transport or signaling were altered. K+ and Ca2+ transporter-encoding genes and the MYB transcription factor were upregulated under salt stress. However, the genes involved in cell wall biosynthesis and secondary metabolism were downregulated. CONCLUSION: Our research identified some important pathways and putative genes involved in salt tolerance in P. macrophyllus and provided clues for elucidating the mechanism of salt tolerance and the utilization of the salt tolerance genes of P. macrophyllus for crop improvement.

Reproductive innovations and pulsed rise in plant complexity.

Morphological complexity is a notable feature of multicellular life, although whether it evolves gradually or in early bursts is unclear. Vascular plant reproductive structures, such as flowers, are familiar examples of complex morphology. In this study, we use a simple approach based on the number of part types to analyze changes in complexity over time. We find that reproductive complexity increased in two pulses separated by ~250 million years of stasis, including an initial rise in the Devonian with the radiation of vascular plants and a pronounced increase in the Late Cretaceous that reflects flowering plant diversification. These pulses are associated with innovations that increased functional diversity, suggesting that shifts in complexity are linked to changes in function regardless of whether they occur early or late in the history of vascular plants.

Light- and hormone-mediated development in non-flowering plants: An overview.

MAIN CONCLUSION: Light, hormones and their interaction regulate different aspects of development in non-flowering plants. They might have played a role in the evolution of different plant groups by conferring specific adaptive evolutionary changes. Plants are sessile organisms. Unlike animals, they lack the opportunity to abandon their habitat in unfavorable conditions. They respond to different environmental cues and adapt accordingly to control their growth and developmental pattern. While phytohormones are known to be internal regulators of plant development, light is a major environmental signal that shapes plant processes. It is plausible that light-hormone crosstalk might have played an important role in plant evolution. But how the crosstalk between light and phytohormone signaling pathways might have shaped the plant evolution is unclear. One of the possible reasons is that flowering plants have been studied extensively in context of plant development, which cannot serve the purpose of evolutionary comparisons. In order to elucidate the role of light, hormone and their crosstalk in the evolutionary adaptation in plant kingdom, one needs to understand various light- and hormone-mediated processes in diverse non-flowering plants. This review is an attempt to outline major light- and phytohormone-mediated responses in non-flowering plant groups such as algae, bryophytes, pteridophytes and gymnosperms.

A full-length transcriptome and gene expression analysis reveal genes and molecular elements expressed during seed development in Gnetum luofuense.

BACKGROUND: Gnetum is an economically important tropical and subtropical gymnosperm genus with various dietary, industrial and medicinal uses. Many carbohydrates, proteins and fibers accumulate during the ripening of Gnetum seeds. However, the molecular mechanisms related to this process remain unknown. RESULTS: We therefore assembled a full-length transcriptome from immature and mature G. luofuense seeds using PacBio sequencing reads. We identified a total of 5726 novel genes, 9061 alternative splicing events, 3551 lncRNAs, 2160 transcription factors, and we found that 8512 genes possessed at least one poly(A) site. In addition, gene expression comparisons of six transcriptomes generated by Illumina sequencing showed that 14,323 genes were differentially expressed from an immature stage to a mature stage with 7891 genes upregulated and 6432 genes downregulated. The expression of 14 differentially expressed transcription factors from the MADS-box, Aux/IAA and bHLH families was validated by qRT-PCR, suggesting that they may have important roles in seed ripening of G. luofuense. CONCLUSIONS: These findings provide a valuable molecular resource for understanding seed development of gymnosperms.

Gymnosperm glandular trichomes: expanded dimensions of the conifer terpenoid defense system.

Glandular trichomes (GTs) are defensive structures that produce and accumulate specialized metabolites and protect plants against herbivores, pathogens, and abiotic stress. GTs have been extensively studied in angiosperms for their roles in defense and biosynthesis of high-value metabolites. In contrast, trichomes of gymnosperms have been described in fossilized samples, but have not been studied in living plants. Here, we describe the characterization of GTs on young stems of a hybrid white spruce. Metabolite and histological analysis of spruce GTs support a glandular function with accumulation of a diverse array of mono-, sesqui- and diterpenes including diterpene methylesters. Methylated diterpenes have previously been associated with insect resistance in white spruce. Headspeace analysis of spruce GTs showed a profile of volatiles dominated by monoterpenes and a highly diverse array of sesquiterpenes. Spruce GTs appear early during shoot growth, prior to the development of a lignified bark and prior to accumulation of terpenes in needles. Spruce GTs may provide an early, terpene-based chemical defense system at a developmental stage when young shoots are particularly vulnerable to foliage and shoot feeding insects, and before the resin duct system characteristic of conifers has fully developed.

Low growth resilience to drought is related to future mortality risk in trees.

Severe droughts have the potential to reduce forest productivity and trigger tree mortality. Most trees face several drought events during their life and therefore resilience to dry conditions may be crucial to long-term survival. We assessed how growth resilience to severe droughts, including its components resistance and recovery, is related to the ability to survive future droughts by using a tree-ring database of surviving and now-dead trees from 118 sites (22 species, >3,500 trees). We found that, across the variety of regions and species sampled, trees that died during water shortages were less resilient to previous non-lethal droughts, relative to coexisting surviving trees of the same species. In angiosperms, drought-related mortality risk is associated with lower resistance (low capacity to reduce impact of the initial drought), while it is related to reduced recovery (low capacity to attain pre-drought growth rates) in gymnosperms. The different resilience strategies in these two taxonomic groups open new avenues to improve our understanding and prediction of drought-induced mortality.

Development of deforestation and land cover database for Bhutan (1930-2014).

Bhutan is a mountainous country located in the Himalayan biodiversity hotspot. This study has quantified the total area under land cover types, estimated the rate of forest cover change, analyzed the changes across forest types, and modeled forest cover change hotpots in Bhutan. The topographical maps and satellite remote sensing images were analyzed to get the spatial patterns of forest and associated land cover changes over the past eight decades (1930-1977-1987-1995-2005-2014). Forest is the largest land cover in Bhutan and constitutes 68.3% of the total geographical area in 2014. Subtropical broad leaved hill forest is predominant type occupies 34.1% of forest area in Bhutan, followed by montane dry temperate (20.9%), montane wet temperate (18.9%), Himalayan moist temperate (10%), and tropical moist sal (8.1%) in 2014. The major forest cover loss is observed in subtropical broad leaved hill forest (64.5 km2) and moist sal forest (9.9 km2) from 1977 to 2014. The deforested areas have mainly been converted into agriculture and contributed for 60.9% of forest loss from 1930 to 2014. In spite of major decline of forest cover in time interval of 1930-1977, there is no net rate of deforestation is recorded in Bhutan since 1995. Forest cover change analysis has been carried out to evaluate the conservation effectiveness in "Protected Areas" of Bhutan. Hotspots that have undergone high transformation in forest cover for afforestation and deforestation were highlighted in the study for conservation prioritisation. Forest conservation policies in Bhutan are highly effective in controlling deforestation as compared to neighboring Asian countries and such service would help in mitigating climate change.

Current trends and future directions in flower development research.

Flowers, the reproductive structures of the approximately 400 000 extant species of flowering plants, exist in a tremendous range of forms and sizes, mainly due to developmental differences involving the number, arrangement, size and form of the floral organs of which they consist. However, this tremendous diversity is underpinned by a surprisingly robust basic floral structure in which a central group of carpels forms on an axis of determinate growth, almost invariably surrounded by two successive zones containing stamens and perianth organs, respectively. Over the last 25 years, remarkable progress has been achieved in describing the molecular mechanisms that control almost all aspects of flower development, from the phase change that initiates flowering to the final production of fruits and seeds. However, this work has been performed almost exclusively in a small number of eudicot model species, chief among which is Arabidopsis thaliana. Studies of flower development must now be extended to a much wider phylogenetic range of flowering plants and, indeed, to their closest living relatives, the gymnosperms. Studies of further, more wide-ranging models should provide insights that, for various reasons, cannot be obtained by studying the major existing models alone. The use of further models should also help to explain how the first flowering plants evolved from an unknown, although presumably gymnosperm-like ancestor, and rapidly diversified to become the largest major plant group and to dominate the terrestrial flora. The benefits for society of a thorough understanding of flower development are self-evident, as human life depends to a large extent on flowering plants and on the fruits and seeds they produce. In this preface to the Special Issue, we introduce eleven articles on flower development, representing work in both established and further models, including gymnosperms. We also present some of our own views on current trends and future directions of the flower development field.

Ontogenetic shifts in plant-plant interactions in a rare cycad within angiosperm communities.

Gymnosperms and angiosperms can co-occur within the same habitats but key plant traits are thought to give angiosperms an evolutionary competitive advantage in many ecological settings. We studied ontogenetic changes in competitive and facilitative interactions between a rare gymnosperm (Dioon sonorense, our target species) and different plant and abiotic neighbours (conspecific-cycads, heterospecific-angiosperms, or abiotic-rocks) from 2007 to 2010 in an arid environment of northwestern Mexico. We monitored survival and growth of seedlings, juveniles, and adults of the cycad Dioon sonorense to evaluate how cycad survival and relative height growth rate (RHGR) responded to intra- and interspecific competition, canopy openness, and nearest neighbour. We tested spatial associations among D. sonorense life stages and angiosperm species and measured ontogenetic shifts in cycad shade tolerance. Canopy openness decreased cycad survival while intraspecific competition decreased survival and RHGR during early ontogeny. Seedling survival was higher in association with rocks and heterospecific neighbours where intraspecific competition was lower. Shade tolerance decreased with cycad ontogeny reflecting the spatial association of advanced stages with more open canopies. Interspecific facilitation during early ontogeny of our target species may promote its persistence in spite of increasing interspecific competition in later stages. We provide empirical support to the long-standing assumption that marginal rocky habitats serve as refugia from angiosperm competition for slow-growing gymnosperms such as cycads. The lack of knowledge of plant-plant interactions in rare or endangered species may hinder developing efficient conservation strategies (e.g. managing for sustained canopy cover), especially under the ongoing land use and climatic changes.

Long-term temporal changes in central European tree phenology (1946-2010) confirm the recent extension of growing seasons.

One of the ways to assess the impacts of climate change on plants is analysing their long-term phenological data. We studied phenological records of 18 common tree species and their 8 phenological phases, spanning 65 years (1946-2010) and covering the area of the Czech Republic. For each species and phenophase, we assessed the changes in its annual means (for detecting shifts in the timing of the event) and standard deviations (for detecting changes in duration of the phenophases). The prevailing pattern across tree species was that since around the year 1976, there has been a consistent advancement of the onset of spring phenophases (leaf unfolding and flowering) and subsequent acceleration of fruit ripening, and a delay of autumn phenophases (leaf colouring and leaf falling). The most considerable shifts in the timing of spring phenophases were displayed by early-successional short-lived tree species. The most pronounced temporal shifts were found for the beginning of seed ripening in conifers with an advancement in this phenophase of up to 2.2 days year⁻¹ in Scots Pine (Pinus sylvestris). With regards to the change in duration of the phenophases, no consistent patterns were revealed. The growing season has extended on average by 23.8 days during the last 35 years. The most considerable prolongation was found in Pedunculate Oak (Quercus robur): 31.6 days (1976-2010). Extended growing season lengths do have the potential to increase growth and seed productivity, but unequal shifts among species might alter competitive relationships within ecosystems.

A phylogenetic comparative study of flowering phenology along an elevational gradient in the Canadian subarctic.

Climate change is affecting high-altitude and high-latitude communities in significant ways. In the short growing season of subarctic habitats, it is essential that the timing and duration of phenological phases match favorable environmental conditions. We explored the time of the first appearance of flowers (first flowering day, FFD) and flowering duration across subarctic species composing different communities, from boreal forest to tundra, along an elevational gradient (600-800 m). The study was conducted on Mount Irony (856 m), North-East Canada (54°90'N, 67°16'W) during summer 2012. First, we quantified phylogenetic signal in FFD at different spatial scales. Second, we used phylogenetic comparative methods to explore the relationship between FFD, flowering duration, and elevation. We found that the phylogenetic signal for FFD was stronger at finer spatial scales and at lower elevations, indicating that closely related species tend to flower at similar times when the local environment is less harsh. The comparatively weaker phylogenetic signal at higher elevation may be indicative of convergent evolution for FFD. Flowering duration was correlated significantly with mean FFD, with later-flowering species having a longer flowering duration, but only at the lowest elevation. Our results indicate significant evolutionary conservatism in responses to phenological cues, but high phenotypic plasticity in flowering times. We suggest that phylogenetic relationships should be considered in the search for predictions and drivers of flowering time in comparative analyses, because species cannot be considered as statistically independent. Further, phenological drivers should be measured at spatial scales such that variation in flowering matches variation in environment.

Palynological composition of a Lower Cretaceous South American tropical sequence: climatic implications and diversity comparisons with other latitudes.

PREMISE OF THE STUDY: Reconstruction of floristic patterns during the early diversification of angiosperms is impeded by the scarce fossil record, especially in tropical latitudes. Here we collected quantitative palynological data from a stratigraphic sequence in tropical South America to provide floristic and climatic insights into such tropical environments during the Early Cretaceous. METHODS: We reconstructed the floristic composition of an Aptian-Albian tropical sequence from central Colombia using quantitative palynology (rarefied species richness and abundance) and used it to infer its predominant climatic conditions. Additionally, we compared our results with available quantitative data from three other sequences encompassing 70 floristic assemblages to determine latitudinal diversity patterns. KEY RESULTS: Abundance of humidity indicators was higher than that of aridity indicators (61% vs. 10%). Additionally, we found an angiosperm latitudinal diversity gradient (LDG) for the Aptian, but not for the Albian, and an inverted LDG of the overall diversity for the Albian. Angiosperm species turnover during the Albian, however, was higher in humid tropics. CONCLUSIONS: There were humid climates in northwestern South America during the Aptian-Albian interval contrary to the widespread aridity expected for the tropical belt. The Albian inverted overall LDG is produced by a faster increase in per-sample angiosperm and pteridophyte diversity in temperate latitudes. However, humid tropical sequences had higher rates of floristic turnover suggesting a higher degree of morphological variation than in temperate regions.

Cretaceous/Paleogene floral turnover in Patagonia: drop in diversity, low extinction, and a Classopollis spike.

Nearly all data regarding land-plant turnover across the Cretaceous/Paleogene boundary come from western North America, relatively close to the Chicxulub, Mexico impact site. Here, we present a palynological analysis of a section in Patagonia that shows a marked fall in diversity and abundance of nearly all plant groups across the K/Pg interval. Minimum diversity occurs during the earliest Danian, but only a few palynomorphs show true extinctions. The low extinction rate is similar to previous observations from New Zealand. The differing responses between the Southern and Northern hemispheres could be related to the attenuation of damage with increased distance from the impact site, to hemispheric differences in extinction severity, or to both effects. Legacy effects of the terminal Cretaceous event also provide a plausible, partial explanation for the fact that Paleocene and Eocene macrofloras from Patagonia are among the most diverse known globally. Also of great interest, earliest Danian assemblages are dominated by the gymnosperm palynomorphs Classopollis of the extinct Mesozoic conifer family Cheirolepidiaceae. The expansion of Classopollis after the boundary in Patagonia is another example of typically Mesozoic plant lineages surviving into the Cenozoic in southern Gondwanan areas, and this greatly supports previous hypotheses of high latitude southern regions as biodiversity refugia during the end-Cretaceous global crisis.

Is iron phloem mobile during senescence in trees? A reinvestigation of Rissmüller's finding of 1874.

As long as 130 years ago Rissmüller reported substantial retranslocation of iron (Fe) from beech leaves (Fagus sylvatica L.) shortly before leaf fall. This rather limited report on Fe retranslocation via the phloem in plants was the reason for this research to study changes in Fe content in individual beech leaves in more detail during the vegetative period. Besides Fe, other micronutrients and particularly Ca and K, well known to differ substantially in phloem mobility, were analysed as mineral nutrient markers. In addition to beech, other deciduous and evergreen species of Angiosperms and Gymnosperms were also studied. As expected, there was no evidence of Ca retranslocation from senescent leaves, while K as a phloem mobile mineral nutrient was retranslocated in fall in deciduous but not in evergreen trees. There was no indication to support Rissmüller's finding of Fe retranslocation in any of the different species studied. From these results, we conclude that natural leaf senescence of trees during late season does not induce retranslocation of Fe and other micronutrients. Possible reasons for the absence of a distinct retranslocation of Fe in the species studied during late season senescence are the lack of a sink activity, as for example the development of seeds in annual plant species (e.g., cereals), or the presence of a root system still active enough to provide Fe and other mineral nutrients for plant demand, and both factors have to be considered in further studies. Reviewing the data in the literature on Fe and Zn retranslocation during senescence, we conclude that in principle both micronutrients are potentially phloem mobile. However, various prerequisites are needed for the occurrence of phloem mobility which were absent in the plant species studied. Regardless of this conclusion, we recommend that in general early published research data need a critical re-evaluation.

Gene family structure, expression and functional analysis of HD-Zip III genes in angiosperm and gymnosperm forest trees.

BACKGROUND: Class III Homeodomain Leucine Zipper (HD-Zip III) proteins have been implicated in the regulation of cambium identity, as well as primary and secondary vascular differentiation and patterning in herbaceous plants. They have been proposed to regulate wood formation but relatively little evidence is available to validate such a role. We characterised and compared HD-Zip III gene family in an angiosperm tree, Populus spp. (poplar), and the gymnosperm Picea glauca (white spruce), representing two highly evolutionarily divergent groups. RESULTS: Full-length cDNA sequences were isolated from poplar and white spruce. Phylogenetic reconstruction indicated that some of the gymnosperm sequences were derived from lineages that diverged earlier than angiosperm sequences, and seem to have been lost in angiosperm lineages. Transcript accumulation profiles were assessed by RT-qPCR on tissue panels from both species and in poplar trees in response to an inhibitor of polar auxin transport. The overall transcript profiles HD-Zip III complexes in white spruce and poplar exhibited substantial differences, reflecting their evolutionary history. Furthermore, two poplar sequences homologous to HD-Zip III genes involved in xylem development in Arabidopsis and Zinnia were over-expressed in poplar plants. PtaHB1 over-expression produced noticeable effects on petiole and primary shoot fibre development, suggesting that PtaHB1 is involved in primary xylem development. We also obtained evidence indicating that expression of PtaHB1 affected the transcriptome by altering the accumulation of 48 distinct transcripts, many of which are predicted to be involved in growth and cell wall synthesis. Most of them were down-regulated, as was the case for several of the poplar HD-Zip III sequences. No visible physiological effect of over-expression was observed on PtaHB7 transgenic trees, suggesting that PtaHB1 and PtaHB7 likely have distinct roles in tree development, which is in agreement with the functions that have been assigned to close homologs in herbaceous plants. CONCLUSIONS: This study provides an overview of HD-zip III genes related to woody plant development and identifies sequences putatively involved in secondary vascular growth in angiosperms and in gymnosperms. These gene sequences are candidate regulators of wood formation and could be a source of molecular markers for tree breeding related to wood properties.

Effects of sap-feeding insect herbivores on growth and reproduction of woody plants: a meta-analysis of experimental studies.

The majority of generalisations concerning plant responses to herbivory are based on studies of natural or simulated defoliation. However, effects caused by insects feeding on plant sap are likely to differ from the effects of folivory. We assessed the general patterns and sources of variation in the effects of sap feeding on growth, photosynthesis, and reproduction of woody plants through a meta-analysis of 272 effect sizes calculated from 52 papers. Sap-feeders significantly reduced growth (-29%), reproduction (-17%), and photosynthesis (-27%); seedlings suffered more than saplings and mature trees. Deciduous and evergreen woody plants did not differ in their abilities to tolerate damage imposed by sap-feeders. Different plant parts, in particular below- and above-ground organs, responded similarly to damage, indicating that sap-feeders did not change the resource allocation in plants. The strongest effects were caused by mesophyll and phloem feeders, and the weakest by xylem feeders. Generalist sap-feeders reduced plant performance to a greater extent than did specialists. Methodology substantially influenced the outcomes of the primary studies; experiments conducted in greenhouses yielded stronger negative effects than field experiments; shorter (<12 months) experiments showed bigger growth reduction in response to sap feeding than longer experiments; natural levels of herbivory caused weaker effects than infestation of experimental plants by sap-feeders. Studies conducted at higher temperatures yielded stronger detrimental effects of sap-feeders on their hosts. We conclude that sap-feeders impose a more severe overall negative impact on plant performance than do defoliators, mostly due to the lower abilities of woody plants to compensate for sap-feeders' damage in terms of both growth and photosynthesis.

Gene expression patterns in seed plant shoot meristems and leaves: homoplasy or homology?

The fossil record reveals that seed plant leaves evolved from ancestral lateral branch systems. Over time, the lateral branch systems evolved to become determinate, planar and eventually laminar. Considering their evolutionary histories, it is instructive to compare the developmental genetics of shoot apical meristems (SAMs) and leaves in extant seed plants. Genetic experiments in model angiosperm species have assigned functions of meristem maintenance, specification of stem cell identity, boundary formation, polarity establishment and primordium initiation to specific genes. Investigation of roles of the same or homologous genes during leaf development has revealed strikingly similar functions in leaves compared to SAMs. Specifically, the marginal blastozone that characterizes many angiosperm leaves appears to function in a manner mechanistically similar to the SAM. We argue here that the similarities may be homologous due to descent from ancestral roles in an ancestral shoot system. Molecular aspects of SAM and leaf development in gymnosperms is largely neglected and could provide insight into seed plant leaf evolution.