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At least 19 records

XYLEM NAC DOMAIN1, an angiosperm NAC transcription factor, inhibits xylem differentiation through conserved motifs that interact with RETINOBLASTOMA‐RELATED

Summary The Arabidopsis thaliana gene XYLEM NAC DOMAIN1 ( XND1 ) is upregulated in xylem tracheary elements. Yet overexpression of XND1 blocks differentiation of tracheary elements. The molecular mechanism of XND1 action was investigated. Phylogenetic and motif analyses indicated that XND1 and its homologs are present only in angiosperms and possess a highly conserved C‐terminal region containing linear motifs (CKII‐acidic, LXCXE, E2F TD ‐like and LXCXE‐mimic) predicted to interact with the cell cycle and differentiation regulator RETINOBLASTOMA‐RELATED (RBR). Protein–protein interaction and functional analyses of XND1 deletion mutants were used to test the importance of RBR‐interaction motifs. Deletion of either the LXCXE or the LXCXE‐mimic motif reduced both the XND1–RBR interaction and XND1 efficacy as a repressor of differentiation, with loss of the LXCXE motif having the strongest negative impacts. The function of the XND1 C‐terminal domain could be partially replaced by RBR fused to the N‐terminal domain of XND1. XND1 also transactivated gene expression in yeast and plants. The properties of XND1, a transactivator that depends on multiple linear RBR‐interaction motifs to inhibit differentiation, have not previously been described for a plant protein. XND1 harbors an apparently angiosperm‐specific combination of interaction motifs potentially linking the general differentiation regulator RBR with a xylem‐specific pathway for inhibition of differentiation.

Zhao, Chengsong↗

The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea

Seagrasses colonized the sea on at least three independent occasions to form the basis of one of the most productive and widespread coastal ecosystems on the planet. Here we report the genome of Zostera marina (L.), the first, to our knowledge, marine angiosperm to be fully sequenced. This reveals unique insights into the genomic losses and gains involved in achieving the structural and physiological adaptations required for its marine lifestyle, arguably the most severe habitat shift ever accomplished by flowering plants. Key angiosperm innovations that were lost include the entire repertoire of stomatal genes, genes involved in the synthesis of terpenoids and ethylene signalling, and genes for ultraviolet protection and phytochromes for far-red sensing. Seagrasses have also regained functions enabling them to adjust to full salinity. Their cell walls contain all of the polysaccharides typical of land plants, but also contain polyanionic, low-methylated pectins and sulfated galactans, a feature shared with the cell walls of all macroalgae and that is important for ion homoeostasis, nutrient uptake and O 2 /CO 2 exchange through leaf epidermal cells. The Z. marina genome resource will markedly advance a wide range of functional ecological studies from adaptation of marine ecosystems under climate warming, to unravelling the mechanisms of osmoregulation under high salinities that may further inform our understanding of the evolution of salt tolerance in crop plants.

59 BASIC BIOLOGICAL SCIENCES↗

Optimal stomatal theory predicts CO 2 responses of stomatal conductance in both gymnosperm and angiosperm trees

Optimal stomatal theory predicts that stomata operate to maximise photosynthesis (A net ) and minimise transpirational water loss to achieve optimal intrinsic water-use efficiency (iWUE). We tested whether this theory can predict stomatal responses to elevated atmospheric CO 2 (eCO 2 ), and whether it can capture differences in responsiveness among woody plant functional types (PFTs). We conducted a meta-analysis of tree studies of the effect of eCO 2 on iWUE and its components A net and stomatal conductance (g s ). We compared three PFTs, using the unified stomatal optimisation (USO) model to account for confounding effects of leaf–air vapour pressure difference (D). We expected smaller g s , but greater A net , responses to eCO 2 in gymnosperms compared with angiosperm PFTs. We found that iWUE increased in proportion to increasing eCO 2 in all PFTs, and that increases in A net had stronger effects than reductions in g s . The USO model correctly captured stomatal behaviour with eCO 2 across most datasets. The chief difference among PFTs was a lower stomatal slope parameter (g 1 ) for the gymnosperm, compared with angiosperm, species. Land surface models can use the USO model to describe stomatal behaviour under changing atmospheric CO 2 conditions.

54 ENVIRONMENTAL SCIENCES↗

Chemical diversity in angiosperms − monoterpene synthases control complex reactions that provide the precursors for ecologically and commercially important monoterpenoids

SUMMARY Monoterpene synthases (MTSs) catalyze the first committed step in the biosynthesis of monoterpenoids, a class of specialized metabolites with particularly high chemical diversity in angiosperms. In addition to accomplishing a rate enhancement, these enzymes manage the formation and turnover of highly reactive carbocation intermediates formed from a prenyl diphosphate substrate. At each step along the reaction path, a cationic intermediate can be subject to cyclization, migration of a proton, hydride, or alkyl group, or quenching to terminate the sequence. However, enzymatic control of ligand folding, stabilization of specific intermediates, and defined quenching chemistry can maintain the specificity for forming a signature product. This review article will discuss our current understanding of how angiosperm MTSs control the reaction environment. Such knowledge allows inferences about the origin and regulation of chemical diversity, which is pertinent for appreciating the role of monoterpenoids in plant ecology but also for aiding commercial efforts that harness the accumulation of these specialized metabolites for the food, cosmetic, and pharmaceutical industries.

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CH↗

Phylogenetically structured traits in root systems influence arbuscular mycorrhizal colonization in woody angiosperms

In this study, there is little quantitative information about the relationship between root traits and the extent of arbuscular mycorrhizal fungi (AMF) colonization. We expected that ancestral species with thick roots will maximize AMF habitat by maintaining similar root traits across root orders (i.e., high root trait integration), whereas more derived species are expected to display a sharp transition from acquisition to structural roots. Moreover, we hypothesized that interspecific morphological differences rather than soil conditions will be the main driver of AMF colonization We analyzed 14 root morphological and chemical traits and AMF colonization rates for the first three root orders of 34 temperate tree species grown in two common gardens. We also collected associated soil to measure the effect of soil conditions on AMF colonization Results Thick-root magnoliids showed less variation in root traits along root orders than more-derived angiosperm groups. Variation in stele:root diameter ratio was the best indicator of AMF colonization within and across root orders. Root functional traits rather than soil conditions largely explained the variation in AMF colonization among species. In conclusion, not only the traits of first order but the entire structuring of the root system varied among plant lineages, suggesting alternative evolutionary strategies of resource acquisition. Understanding evolutionary pathways in below ground organs could open new avenues to understand tree species influence on soil carbon and nutrient cycling.

59 BASIC BIOLOGICAL SCIENCES↗

Testing for the Genomic Footprint of Conflict Between Life Stages in an Angiosperm and Moss Species

Abstract The maintenance of genetic variation by balancing selection is of considerable interest to evolutionary biologists. An important but understudied potential driver of balancing selection is antagonistic pleiotropy between diploid and haploid stages of the plant life cycle. Despite sharing a common genome, sporophytes (2n) and gametophytes (n) may undergo differential or even opposing selection. Theoretical work suggests antagonistic pleiotropy between life stages can generate balancing selection and maintain genetic variation. Despite the potential for far-reaching consequences of gametophytic selection, empirical tests of its pleiotropic effects (neutral, synergistic, or antagonistic) on sporophytes are generally lacking. Here, we examined the population genomic signals of selection across life stages in the angiosperm Rumex hastatulus and the moss Ceratodon purpureus. We compared gene expression between life stages and sexes, combined with neutral diversity statistics and the analysis of the distribution of fitness effects. In contrast to what would be predicted under balancing selection due to antagonistic pleiotropy, we found that unbiased genes between life stages were under stronger purifying selection, likely explained by a predominance of synergistic pleiotropy between life stages and strong purifying selection on broadly expressed genes. In addition, we found that 30% of candidate genes under balancing selection in R. hastatulus were located within inversion polymorphisms. Our findings provide novel insights into the genome-wide characteristics and consequences of plant gametophytic selection.

Evolutionary Biology↗

A test of the hydraulic vulnerability segmentation hypothesis in angiosperm and conifer tree species

Water transport from soils to the atmosphere is critical for plant growth and survival. However, we have a limited understanding about many portions of the whole-tree hydraulic pathway, because the vast majority of published information is on terminal branches. Our understanding of mature tree trunk hydraulic physiology, in particular, is limited. The hydraulic vulnerability segmentation hypothesis (HVSH) stipulates that distal portions of the plant (leaves, branches and roots) should be more vulnerable to embolism than trunks, which are non-redundant organs that require a massive carbon investment. In the current study, we compared vulnerability to loss of hydraulic function, leaf and xylem water potentials and the resulting hydraulic safety margins (in relation to the water potential causing 50% loss of hydraulic conductivity) in leaves, branches, trunks and roots of four angiosperms and four conifer tree species. Across all species, our results supported strongly the HVSH as leaves and roots were less resistant to embolism than branches or trunks. However, branches were consistently more resistant to embolism than any other portion of the plant, including trunks. Also, calculated whole-tree vulnerability to hydraulic dysfunction was much greater than vulnerability in branches. This was due to hydraulic dysfunction in roots and leaves at less negative water potentials than those causing branch or trunk dysfunction. Leaves and roots had narrow or negative hydraulic safety margins, but trunks and branches maintained positive safety margins. By using branch-based hydraulic information as a proxy for entire plants, much research has potentially overestimated embolism resistance, and possibly drought tolerance, for many species. This study highlights the necessity to reconsider past conclusions made about plant resistance to drought based on branch xylem only. As a result, this study also highlights the necessity for more research of whole-plant hydraulic physiology to better understand strategies of plant drought tolerance and the critical control points within the hydraulic pathway.

59 BASIC BIOLOGICAL SCIENCES↗

Evolutionary analysis of the LORELEI gene family in plants reveals regulatory subfunctionalization

Abstract A signaling complex comprising members of the LORELEI (LRE)-LIKE GPI-anchored protein (LLG) and Catharanthus roseus RECEPTOR-LIKE KINASE 1-LIKE (CrRLK1L) families perceive RAPID ALKALINIZATION FACTOR (RALF) peptides and regulate growth, reproduction, immunity, and stress responses in Arabidopsis (Arabidopsis thaliana). Genes encoding these proteins are members of multigene families in most angiosperms and could generate thousands of signaling complex variants. However, the links between expansion of these gene families and the functional diversification of this critical signaling complex as well as the evolutionary factors underlying the maintenance of gene duplicates remain unknown. Here, we investigated LLG gene family evolution by sampling land plant genomes and explored the function and expression of angiosperm LLGs. We found that LLG diversity within major land plant lineages is primarily due to lineage-specific duplication events, and that these duplications occurred both early in the history of these lineages and more recently. Our complementation and expression analyses showed that expression divergence (i.e. regulatory subfunctionalization), rather than functional divergence, explains the retention of LLG paralogs. Interestingly, all but one monocot and all eudicot species examined had an LLG copy with preferential expression in male reproductive tissues, while the other duplicate copies showed highest levels of expression in female or vegetative tissues. The single LLG copy in Amborella trichopoda is expressed vastly higher in male compared to in female reproductive or vegetative tissues. We propose that expression divergence plays an important role in retention of LLG duplicates in angiosperms.

Plant Sciences↗

Cytochrome b5 diversity in green lineages preceded the evolution of syringyl lignin biosynthesis

Abstract Lignin production marked a milestone in vascular plant evolution, and the emergence of syringyl (S) lignin is lineage specific. S-lignin biosynthesis in angiosperms, mediated by ferulate 5-hydroxylase (F5H, CYP84A1), has been considered a recent evolutionary event. F5H uniquely requires the cytochrome b5 protein CB5D as an obligatory redox partner for catalysis. However, it remains unclear how CB5D functionality originated and whether it coevolved with F5H. We reveal here the ancient evolution of CB5D-type function supporting F5H-catalyzed S-lignin biosynthesis. CB5D emerged in charophyte algae, the closest relatives of land plants, and is conserved and proliferated in embryophytes, especially in angiosperms, suggesting functional diversification of the CB5 family before terrestrialization. A sequence motif containing acidic amino residues in Helix 5 of the CB5 heme-binding domain contributes to the retention of CB5D function in land plants but not in algae. Notably, CB5s in the S-lignin–producing lycophyte Selaginella lack these residues, resulting in no CB5D-type function. An independently evolved S-lignin biosynthetic F5H (CYP788A1) in Selaginella relies on NADPH-dependent cytochrome P450 reductase as sole redox partner, distinct from angiosperms. These results suggest that angiosperm F5Hs coopted the ancient CB5D, forming a modern cytochrome P450 monooxygenase system for aromatic ring meta-hydroxylation, enabling the reemergence of S-lignin biosynthesis in angiosperms.

59 BASIC BIOLOGICAL SCIENCES↗

Gravitropisms and reaction woods of forest trees – evolution, functions and mechanisms

Summary The woody stems of trees perceive gravity to determine their orientation, and can produce reaction woods to reinforce or change their position. Together, graviperception and reaction woods play fundamental roles in tree architecture, posture control, and reorientation of stems displaced by wind or other environmental forces. Angiosperms and gymnosperms have evolved strikingly different types of reaction wood. Tension wood of angiosperms creates strong tensile force to pull stems upward, while compression wood of gymnosperms creates compressive force to push stems upward. In this review, the general features and evolution of tension wood and compression wood are presented, along with descriptions of how gravitropisms and reaction woods contribute to the survival and morphology of trees. An overview is presented of the molecular and genetic mechanisms underlying graviperception, initial graviresponse and the regulation of tension wood development in the model angiosperm, Populus . Critical research questions and new approaches are discussed. Contents Summary 790 I. Introduction 790 II. General features and evolution of reaction woods of angiosperms and gymnosperms 792 III. Adaptive significance of reaction woods, including relationship to form 795 IV. Perception and primary responses to gravity and physical stimuli in woody stems 797 V. Mechanisms regulating developmental changes in reaction woods 798 VI. Research questions and new research approaches 800 VII. Conclusions 800 Acknowledgements 800 References 800

Groover, Andrew↗

Bayesian phylogeny of sucrose transporters: ancient origins, differential expansion and convergent evolution in monocots and dicots

Sucrose transporters (SUTs) are essential for the export and efficient movement of sucrose from source leaves to sink organs in plants. The angiosperm SUT family was previously classified into three or four distinct groups, Types I, II (subgroup IIB), and III, with dicot-specific Type I and monocot-specific Type IIB functioning in phloem loading. To shed light on the underlying drivers of SUT evolution, Bayesian phylogenetic inference was undertaken using 41 sequenced plant genomes, including seven basal lineages at key evolutionary junctures. Our analysis supports four phylogenetically and structurally distinct SUT subfamilies, originating from two ancient groups (AG1 and AG2) that diverged early during terrestrial colonization. In both AG1 and AG2, multiple intron acquisition events in the progenitor vascular plant established the gene structures of modern SUTs. Tonoplastic Type III and plasmalemmal Type II represent evolutionarily conserved descendants of AG1 and AG2, respectively. Type I and Type IIB were previously thought to evolve after the dicot-monocot split. We show, however, that divergence of Type I from Type III SUT predated basal angiosperms, likely associated with evolution of vascular cambium and phloem transport. Type I SUT was subsequently lost in monocots along with vascular cambium, and independent evolution of Type IIB coincided with modified monocot vasculature. Both Type I and Type IIB underwent lineage-specific expansion. In multiple unrelated taxa, the newly-derived SUTs exhibit biased expression in reproductive tissues, suggesting a functional link between phloem loading and reproductive fitness. Convergent evolution of Type land Type IIB for SUT function in phloem loading and reproductive organs supports the idea that differential vascular development in dicots and monocots is a strong driver for SUT family evolution in angiosperms.

59 BASIC BIOLOGICAL SCIENCES↗

The uncharacterized gene EVE contributes to vessel element dimensions in Populus

The radiation of angiosperms led to the emergence of the vast majority of today’s plant species and all our major food crops. Their extraordinary diversification occurred in conjunction with the evolution of a more efficient vascular system for the transport of water, composed of vessel elements. The physical dimensions of these water-conducting specialized cells have played a critical role in angiosperm evolution; they determine resistance to water flow, influence photosynthesis rate, and contribute to plant stature. However, the genetic factors that determine their dimensions are unclear. Here we show that a previously uncharacterized gene, ENLARGED VESSEL ELEMENT ( EVE ) , contributes to the dimensions of vessel elements in Populus , impacting hydraulic conductivity. Our data suggest that EVE is localized in the plasma membrane and is involved in potassium uptake of differentiating xylem cells during vessel development. In plants, EVE first emerged in streptophyte algae, but expanded dramatically among vessel-containing angiosperms. The phylogeny, structure and composition of EVE indicates that it may have been involved in an ancient horizontal gene-transfer event.

59 BASIC BIOLOGICAL SCIENCES↗

Genome organization and botanical diversity

Abstract The rich diversity of angiosperms, both the planet's dominant flora and the cornerstone of agriculture, is integrally intertwined with a distinctive evolutionary history. Here, we explore the interplay between angiosperm genome organization and botanical diversity, empowered by genomic approaches ranging from genetic linkage mapping to analysis of gene regulation. Commonality in the genetic hardware of plants has enabled robust comparative genomics that has provided a broad picture of angiosperm evolution and implicated both general processes and specific elements in contributing to botanical diversity. We argue that the hardware of plant genomes—both in content and in dynamics—has been shaped by selection for rather substantial differences in gene regulation between plants and animals such as maize and human, organisms of comparable genome size and gene number. Their distinctive genome content and dynamics may reflect in part the indeterminate development of plants that puts strikingly different demands on gene regulation than in animals. Repeated polyploidization of plant genomes and multiplication of individual genes together with extensive rearrangement and differential retention provide rich raw material for selection of morphological and/or physiological variations conferring fitness in specific niches, whether natural or artificial. These findings exemplify the burgeoning information available to employ in increasing knowledge of plant biology and in modifying selected plants to better meet human needs.

Biochemistry & Molecular Biology↗

Fine root morphology is phylogenetically structured, but nitrogen is related to the plant economics spectrum in temperate trees

Summary Plant functional traits have revealed trade‐offs related to life‐history adaptations, geographical distributions, and ecosystem processes. Fine roots are essential in plant resource acquisition and play an important role in soil carbon cycling. Nonetheless, root trait variation is still poorly quantified and rarely related to the rest of the plant. We examined chemical and morphological traits of 34 temperate arbuscular mycorrhizal tree species, representing three main angiosperm clades (super‐orders asterid, magnoliid and rosid). We tested to what extent fine root chemical and morphological traits were correlated similarly to the leaf economical spectrum ( LES ) or were structured by ancestral affiliations among species. Root traits did not display the same trade‐offs as leaves (e.g. specific root length was not correlated with root N, whereas specific leaf area was correlated with leaf N). Moreover, 75% of below‐ground traits were phylogenetically structured according to Pagel's λ and Abouheif's C mean autocorrelation tests, as opposed to 28% of above‐ground traits. Magnoliids showed thicker, less branched roots than asterids or rosids, but rosid roots exhibited lower N and higher non‐acid‐hydrolysable (e.g. lignin) content than other species. In contrast, leaf traits did not differ significantly among super‐orders. At the whole‐tree level, chemical traits such as nitrogen tissue content and lignin content were correlated between above and below‐ground organs. The distribution of root traits in woody temperate trees was better explained by shared ancestry than by the nutrient content and structural trade‐offs expected by the LES hypothesis. Root chemistry and morphology differed substantially among species belonging to different super‐orders, suggesting deep divergences in resource acquisition strategies among major angiosperm groups. Although we found partial support for the idea of whole‐plant integration based on corresponding nitrogen content across all organs (i.e. a plant economics spectrum), our study stresses phylogenetic affiliation as the primary driver of root trait distributions among angiosperms, a pattern that could be easily overlooked based solely on above‐ground observations.

Valverde‐Barrantes, Oscar J.↗