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Introduction.Aphanorrhegma (Physcomitrella) patens(Hedw.) Lindb. is an attractive model system for comparative analyses of leaf development because it evolved leaves (phyllids) independently toflowering plants, yet its genome contains homologues of many gene families that regulate angiosperm leaf development. In addition,A. patensphyllids are primarily a single cell layer thick, making it simple to identify the cellular basis of defects that perturb shape. Identification of gene functions in shape determination depends on like-for- like comparison of mutant versus wild-type plants.Key results.Here we show that, if heteroblasty is not perturbed, such comparisons should use phyllid L13 or above in the heteroblastic series, and fully expanded phyllids above P7 in the developmental series. Using a quantitative approach, we show that heteroblastic size variation reflects differences in cell proliferation rather than cell size and shape. A comparison of control topinA pinBmutant phyllid development verifies that PIN proteins promote cell proliferation and suppress expansion to determine phyllid shape.Conclusion.The results and approach that we have generated will be applicable to any study of A. patensphyllid development to reveal the cellular basis of phyllid size and shape variations.

International audience; The diverse forms of today's dominant vascular plant flora are generated by the sustained proliferative activity of sporophyte meristems at plants' shoot and root tips, a trait known as indeterminacy [1]. Bryophyte sister lineages to the vascular plants lack such indeterminate meristems and have an overall sporophyte form comprising a single small axis that ceases growth in the formation of a reproductive sporangium [1]. Genetic mechanisms regulating indeterminacy are well characterized in flowering plants, involving a feedback loop between class I KNOX genes and cytokinin [2, 3], and class I KNOX expression is a conserved feature of vascular plant meristems [4]. The transition from determinate growth to indeterminacy during evolution was a pre-requisite to vascular plant diversification, but mechanisms enabling the innovation of indeterminacy are unknown [5]. Here, we show that class I KNOX gene activity is necessary and sufficient for axis extension from an intercalary region of determinate moss shoots. As in Arabidopsis, class I KNOX activity can promote cytokinin biosynthesis by an ISOPENTENYL TRANSFERASE gene, PpIPT3. PpIPT3 promotes axis extension, and PpIPT3 and exogenously applied cytokinin can partially compensate for loss of class I KNOX function. By outgroup comparison, the results suggest that a pre-existing KNOX-cytokinin regulatory module was recruited into vascular plant shoot meristems during evolution to promote indeterminacy, thereby enabling the radiation of vascular plant shoot forms.

Contents 545 I. 545 II. 546 III. 546 IV. 548 V. 548 VI. 549 VII. 549 Acknowledgements 549 References 549 SUMMARY: Branching is one of the most striking aspects of land plant architecture, affecting resource acquisition and yield. Polar auxin transport by PIN proteins is a primary determinant of flowering plant branching patterns regulating both branch initiation and branch outgrowth. Several lines of experimental evidence suggest that PIN-mediated polar auxin transport is a conserved regulator of branching in vascular plant sporophytes. However, the mechanisms of branching and auxin transport and relationships between the two are not well known outside the flowering plants, and the paradigm for PIN-regulated branching in flowering plants does not fit bryophyte gametophytes. The evidence reviewed here suggests that divergent auxin transport routes contributed to the diversification of branching forms in distinct land plant lineages.

Plant evo-devo research aims to identify the nature of genetic change underpinning the evolution of diverse plant forms. A transcriptomic study comparing gene expression profiles in the meristematic shoot tips of three distantly related vascular plants suggests that different genes were recruited to regulate similar meristematic processes during evolution.

Plant microbial fuel cells are a recently developed technology that exploits photosynthesis in vascular plants by harnessing solar energy and generating electrical power. In this study, the model moss species Physcomitrella patens , and other environmental samples of mosses, have been used to develop a non-vascular bryophyte microbial fuel cell (bryoMFC). A novel three-dimensional anodic matrix was successfully created and characterized and was further tested in a bryoMFC to determine the capacity of mosses to generate electrical power. The importance of anodophilic microorganisms in the bryoMFC was also determined. It was found that the non-sterile bryoMFCs operated with P. patens delivered over an order of magnitude higher peak power output (2.6 ± 0.6 µW m −2 ) than bryoMFCs kept in near-sterile conditions (0.2 ± 0.1 µW m −2 ). These results confirm the importance of the microbial populations for delivering electrons to the anode in a bryoMFC. When the bryoMFCs were operated with environmental samples of moss (non-sterile) the peak power output reached 6.7 ± 0.6 mW m −2 . The bryoMFCs operated with environmental samples of moss were able to power a commercial radio receiver or an environmental sensor (LCD desktop weather station).

In common with most Old World Gesneriaceae; Streptocarpus Lindl. shows anisocotylous growth, i.e., the continuous growth of one cotyledon after germination. Linked to this phenomenon is an unorthodox behaviour of the shoot apical meristem (SAM) that determines the growth pattern of acaulescent species (subgenus Streptocarpus). In contrast caulescent species develop a conventional central post-embryonic SAM (mainly subgenus Streptocarpella). We used S. rexii Lindl. as a model to investigate anisocotyly and meristem initiation in Streptocarpus by using histological techniques and analyses of the expression pattern of the meristematic marker SrSTM1 during ontogeny. In contrast to Arabidopsis thaliana (L.) Heynh., S. rexii does not establish a SAM during embryogenesis, and the first evidence of a SAM-like structure occurs during post-embryonic development on the axis (the petiolode) between the two cotyledons. The expression pattern of SrSTM1 suggests a function in maintaining cell division activity in the cotyledons before becoming localized in the basal meristem, initially at the proximal ends of both cotyledons, later at the base of the continuously growing macrocotyledon, and the groove meristem on the petiolode. The latter is equivalent to a displaced SAM seemingly originating de novo under the influence of endogenous factors. Applied cytokinin retains SrSTM1expression in the small cotyledon, thus promoting isocotyly and re-establishment of a central post-embryonic SAM. Hormone-dependent delocalization of the process of meristem development could underlie anisocotyly and the unorthodox SAM formation in Streptocarpus.

Shoot branching is a primary contributor to plant architecture, evolving independently in flowering plant sporophytes and moss gametophytes. Mechanistic understanding of branching is largely limited to flowering plants such as Arabidopsis, which have a recent evolutionary origin. We show that in gametophytic shoots of Physcomitrella, lateral branches arise by re-specification of epidermal cells into branch initials. A simple model co-ordinating the activity of leafy shoot tips can account for branching patterns, and three known and ancient hormonal regulators of sporophytic branching interact to generate the branching pattern- auxin, cytokinin and strigolactone. The mode of auxin transport required in branch patterning is a key divergence point from known sporophytic pathways. Although PIN-mediated basipetal auxin transport regulates branching patterns in flowering plants, this is not so in Physcomitrella, where bi-directional transport is required to generate realistic branching patterns. Experiments with callose synthesis inhibitors suggest plasmodesmal connectivity as a potential mechanism for transport. DOI: http://dx.doi.org/10.7554/eLife.06808.001, eLife digest Most land plants have shoots that form branches and plants can regulate when and where they grow these branches to best exploit their environment. Plants with flowers and the more ancient mosses both have branching shoots, but these two groups of plants evolved to grow in this way independently of each other. Most studies on shoot branching have focused on flowering plants and so it is less clear how branching works in mosses. Three plant hormones—called auxin, cytokinin and strigolactone—control shoot branching in flowering plants. Auxin moves down the main shoot of the plant to prevent new branches from forming. This movement is controlled by the PIN proteins and several other families of proteins. On the other hand, cytokinin promotes the growth of new branches; and strigolactone can either promote or inhibit shoot branching depending on how the auxin is travelling around the plant. Coudert, Palubicki et al. studied shoot branching in a species of moss called Physcomitrella patens. The experiments show that cells on the outer surface of the main shoot are essentially reprogrammed to become so-called ‘branch initials’, which will then develop into new branches. Next, Coudert, Palubicki et al. made a computational model that was able to simulate the pattern of shoot branching in the moss. Further experiments supported the predictions made by the model. Coudert, Palubicki et al. found that, as in flowering plants, auxin from the tip of the main shoot suppresses branching in the moss, and cytokinin promotes branching. The experiments also showed that strigolactone inhibits shoot branching, but its role is restricted to the base of the shoots. The model predicts that, unlike in flowering plants, auxin must flow in both directions in moss shoots to produce the observed patterns of shoot branching. Also, the experiments suggest that the PIN proteins and another group of proteins that control the movement of auxin do not regulate shoot branching in moss. Instead, it appears that auxin may move through microscopic channels that link one moss cell to the next. Coudert, Palubicki et al.'s findings suggest that both flowering plants and mosses have evolved to use the same three hormones to control shoot branching, but that these hormones interact in different ways. One key next step will be to find out how auxin is transported during shoot branching in moss by manipulating the opening of the channels between the cells. A further challenge will be to find out the precise details of how the hormones control the activity of the branch initial cells. DOI: http://dx.doi.org/10.7554/eLife.06808.002

The morphology of plant fossils from the Rhynie chert has generated longstanding questions about vascular plant shoot and leaf evolution, for instance, which morphologies were ancestral within land plants, when did vascular plants first arise and did leaves have multiple evolutionary origins? Recent advances combining insights from molecular phylogeny, palaeobotany and evo–devo research address these questions and suggest the sequence of morphological innovation during vascular plant shoot and leaf evolution. The evidence pinpoints testable developmental and genetic hypotheses relating to the origin of branching and indeterminate shoot architectures prior to the evolution of leaves, and demonstrates underestimation of polyphyly in the evolution of leaves from branching forms in ‘telome theory’ hypotheses of leaf evolution. This review discusses fossil, developmental and genetic evidence relating to the evolution of vascular plant shoots and leaves in a phylogenetic framework.This article is part of a discussion meeting issue ‘The Rhynie cherts: our earliest terrestrial ecosystem revisited’.

Floral diversity in Streptocarpus and Saintpaulia can be classified into six distinct types on the basis of quantitative variation. Species are differentiated by overall flower size and by corolla lobe size in relation to corolla tube opening size, characteristics implicated in pollination ecology. Saintpaulia has a very short corolla tube and yellow protruding anthers, strikingly different from Streptocarpus , and probably associated with buzz pollination. Some species of Streptocarpus and all species of Saintpaulia are enantiostylous, a feature often linked to buzz pollination. Mapping of these floral characters onto a molecular phylogeny based on ITS sequence data showed that inStreptocarpus flower size evolved from small to large, with reversals in four species. The putatively bee pollinated ‘open-tubed’ type had two independent origins, and the putatively lepidopteran-pollinated ‘keyhole’ type had four separate origins. Enantiostyly had one or two origins. The degree of zygomorphy varies withinStreptocarpus/Saintpaulia. The most extreme difference is between Saintpaulia ionantha and aSaintpaulia peloric cultivar. The developmental basis of floral variation was compared using SEM in three very different types: Streptocarpus primulifolius, Saintpaulia ionantha and a Saintpaulia peloric cultivar. Differences in corolla tube length and zygomorphy are established very early in flower development. Small, early changes in flower development establish major changes in mature floral morphology.

Sexual eukaryotes generate gametes using a specialized cell division called meiosis that serves both to halve the number of chromosomes and to reshuffle genetic variation present in the parent. The nature and mechanism of the meiotic cell division in plants and its effect on genetic variation are reviewed here. As flowers are the site of meiosis and fertilization in angiosperms, meiotic control will be considered within this developmental context. Finally, we review what is known about the control of meiosis in green algae and non-flowering land plants and discuss evolutionary transitions relating to meiosis that have occurred in the lineages giving rise to the angiosperms.

Background: Land plants evolved from aquatic algae more than 450 million years ago. Algal sisters of land plants grow through the activity of apical initial cells that cleave either in one plane to generate filaments or in two planes to generate mats. Acquisition of the capacity for cell cleavage in three planes facilitated the formation of upright bushy body plans and enabled the invasion of land. Evolutionary transitions between filamentous, planar, and bushy growth are mimicked within moss life cycles. Results: We have developed lineage analysis techniques to assess how transitions between growth forms occur in the moss Physcomitrella patens. We show that initial cells giving rise either to new filaments or bushy shoots are frequently juxtaposed on a single parent filament, suggesting a role for short-range cues in specifying differences in cell fate. Shoot initials cleave four times to establish a tetrahedral shape and subsequently cleave in three planes, generating bushy growth. Asymmetric and self-replacing divisions from the tetrahedral initial generate leaf initials that divide asymmetrically to self-replace and to produce daughter cells with restricted fate. The cessation of division in the leaf is distributed unevenly and contributes to final leaf shape. Conclusions: In contrast to flowering plants, changes in body plan in P. patens are regulated by cues acting at the level of single cells and are mediated through asymmetric divisions. Genetic mechanisms regulating shoot and leaf development in P. patens are therefore likely to differ substantially from mechanisms operating in plants with more recent evolutionary origins.

Pseudomonas fluorescens SBW25 is a plant growth-promoting bacterium that efficiently colonizes the leaf surfaces and rhizosphere of a range of plants. Previous studies have identified a putative plant-induced nitrilase gene (pinA) in P. fluorescens SBW25 that is expressed in the rhizosphere of sugar beet plants. Nitrilase enzymes have been characterised in plants, bacteria and fungi and are thought to be important in detoxification of nitriles, utilisation of nitrogen and synthesis of plant hormones. We reveal that pinA is a NIT4-type nitrilase that catalyses the hydrolysis of beta-cyano-L-alanine, a nitrile common in the plant environment and an intermediate in the cyanide detoxification pathway in plants. In plants cyanide is converted to beta-cyano-L-alanine, which is subsequently detoxified to aspartic acid and ammonia by NIT4. In P. fluorescens SBW25 pinA is induced in the presence of beta-cyano-L-alanine, and the beta-cyano-L-alanine precursors cyanide and cysteine. pinA allows P. fluorescens SBW25 to use beta-cyano-L-alanine as a nitrogen source and to tolerate toxic concentrations of this nitrile. In addition, pinA is shown to complement a NIT4 mutation in Arabidopsis thaliana, enabling plants to grow in concentrations of beta-cyano-L-alanine that would otherwise prove lethal. Interestingly, over-expression of pinA in wild-type A. thaliana not only resulted in increased growth in high concentrations of beta-cyano-L-alanine, but also resulted in increased root elongation in the absence of exogenous beta-cyano-L-alanine, demonstrating that beta-cyano-L-alanine nitrilase activity can have a significant effect on root physiology and root development.

A major transition in land plant evolution was from growth in water to growth on land. This transition necessitated major morphological innovations that were accompanied by the development of three-dimensional apical growth. In extant land plants, shoot growth occurs from groups of cells at the apex known as meristems. In different land plant lineages, meristems function in different ways to produce distinct plant morphologies, yet our understanding of the developmental basis of meristem function is limited to the most recently diverged angiosperms. To redress this balance, we have examined meristem function in the lycophyte Selaginella kraussiana. Using a clonal analysis, we show that S. kraussiana shoots are derived from the activity of two short-lived apical initials that facilitate the formation of four axes of symmetry in the shoot. Leaves are initiated from just two epidermal cells, and the mediolateral leaf axis is the first to be established. This pattern of development differs from that seen in flowering plants. These differences are discussed in the context of the development and evolution of diverse land plant forms.

Vascular plants evolved in the Middle to Late Silurian period, about 420 million years ago. The fossil record indicates that these primitive plants had branched stems with sporangia but no leaves. Leaf-like lateral outgrowths subsequently evolved on at least two independent occasions. In extant plants, these events are represented by microphyllous leaves in lycophytes (clubmosses, spikemosses and quillworts) and megaphyllous leaves in euphyllophytes (ferns, gymnosperms and angiosperms). Our current understanding of how leaves develop is restricted to processes that operate during megaphyll formation. Because microphylls and megaphylls evolved independently, different mechanisms might be required for leaf formation. Here we show that this is not so. Gene expression data from a microphyllous lycophyte, phylogenetic analyses, and a cross-species complementation experiment all show that a common developmental mechanism can underpin both microphyll and megaphyll formation. We propose that this mechanism might have operated originally in the context of primitive plant apices to facilitate bifurcation. Recruitment of this pathway to form leaves occurred independently and in parallel in different plant lineages.