Abstract
The study of plant evolution and development in a phylogenetic context has accelerated research advances in both areas over the last decade. The addition of a robust phylogeny for plant taxa based on DNA as well as morphology has given a strong context for this research. Genetics and genomics, including sequencing of many genes, and a better understanding of non-genetic, responsive changes, by plants have increased knowledge of how the different body forms of plants have arisen. Here, I overview the papers in this Special Issue of Annals of Botany on Morphological Adaptation, bringing together a range of papers that link phylogeny and morphology. These lead to models of development and functional adaptation across a range of plant systems, with implications for ecology and ecosystems, as well as development and evolution.
INTRODUCTION
The study of evolution and development (evo-devo) has advanced plant research including speciation (Fernández-Mazuecos and Glover 2017); and as Theodore Dobzhansky stated in 1973, ‘nothing makes sense except in the light of evolution’. But what options are there for plant architecture to evolve – from the gene to cellular to organ and on to whole plant and ecosystem level? As suggested in the mind-map of Fig. 1, we are now in a good position to exploit data from morphological and genetic studies to understand the key processes of evolution and development, taking those results to find their impact on ecology and ecosystems. The papers in this special issue cover a diverse range of species, organs (related to leaves, roots and flowers) and approaches (from advanced microscopy to DNA fingerprinting), to show how modern plant studies can be integrated to lead to models of evolution and understand plant development in the broadest context.
Plant adaptation arises from their morphology, itself a product of evolution and development. In this figure, the aspects and interactions of research at different levels are shown, with the work having implications across botany, including understanding plant phylogeny and speciation, and for ecology and ecosystems.
FUNCTIONAL PLANT ARCHITECTURE AND DEVELOPMENT
Introductory botany courses (‘Botany 101’) teach us that the shoot apical meristem (SAM) is critical to determining plant architecture including leaf phyllotaxis, branching and the transition to flowering. Schnablova et al. (2017) take a comparative approach, linking evolution with SAM characters. They analyse the SAM of no less than 104 different perennial herbaceous angiosperm species, recognizing the ecological importance of variation in plant body form arising from the SAM. Notably, cell number at the SAM is linked to most organ traits, with the other key SAM parameter of cell size only being strongly correlated with seed mass. Given that cell size and cell number (or cell expansion and cell division) are important factors in determining organ sizes and thus whole plant traits, and both arise developmentally at the meristem, this broad study is important in linking SAM parameters to the parameters of the organs developing from it. I anticipate that their data will be used to find many additional and important correlations with development, and perhaps the developmental basis of selection for different growth patterns in species adapted to different environments.
A very large meta-analysis by Hodgson et al. (2017) also focussed on modelling trade-offs related to development, starting from the meristem, and considering seed and leaf size, ecological specialization and plant life histories. Again, a comparative approach is critical to their study, involving more than 2400 species (from work by no less than 23 authors of the paper). Their research is able to link the size attributes of plants (focussing on leaf size) with function and habitat. Using the repetitive units of plant growth – phytomers – Hodgson et al. (2017) are able to conclude that allometrically constrained traits lead to ecological specialization. Their work provides broad support for the seed-phytomer-leaf (SPL) theoretical model integrating the pattern of development of the shoot with seed and leaf development: perhaps treating these aspects of development as the functional glue linking propagation and taxonomy with ecology.
ADAPTATION AND MORPHOLOGY
Adaptation involves both physiology and morphology, and may be genetic or developmental in origin. Beyschlag and Zotz (2017) address a particularly extreme developmental change in Tillandsioid bormeliads, where individuals transform from small plants with narrow leaves to plants that form tanks and store water at the bases of broad leaves. Their paper shows the value of modelling and exploits comparisons between two species adapted to exposed, sunny sites and two from the understory. The modelling addresses both plant water relations and light interception by leaves, factors changing enormously between the two life forms. The model suggests that the plants follow a near-optimum strategy for optimizing leaf photosynthesis while exploiting the ‘water-storage tank’ to counteract the intermittent water supply available to the epiphyte in tree crowns.
A second paper considers differential development with different forms seen in one organism. The study of Slate et al. (2017) shows sex-specific variation in cell, leaf and photochemical traits in the moss Ceratodon. Notably, the female plants (the gametophytes of mosses) had larger, thicker leaves than males with consequences for resource allocation and biotic interactions. However, of the three populations they studied, two had more males and one had more females, hard to explain in view of the high sexual dimorphism. So the consequences of the morphological differences must require further studies of plant fitness of two dimorphic sexes under different conditions.
Annals of Botany has regular Special Issues on Root Biology, including fundamental studies of root anatomy and growth (for the latest see Ryan et al., 2016). Three papers in this Special Issue examine important features of root cell biology as they relate to morphological adaptation and the function of the root. Leite et al. (2017) gives new information about role of the cell wall and cell death (apoptosis) in the formation of intercellular spaces in aerenchyma, maintaining mechanical strength and structural stability while 40% of the root is gas spaces. Soukup et al. (2017) discuss another component of some cell walls that give mechanical stability. Silica aggregates are incorporated in the tertiary wall at pre-determined sites formed during cell development, and silica aggregates may form at these sites even when silicon is only available late in development. Their model takes account of the contrasting hydrophobicity of two modifications of the cell wall architecture, silicification and lignification. These two components both provide stiffness, but the authors suggest that their specific distribution in cell walls affects water movement, helping sustain the plant under adverse environmental conditions.
Morphology has always been important to taxonomy, for inferring phylogeny and understanding plant growth. However, Zotz et al. (2017) in the third root related paper of this Special Issue, point out two problems with many previous studies of the velamen radicum, a structure of the root epidermis, reported as an ‘adaptation’ largely associated with ‘epiphytic orchids’. Mapping the occurrence of the velamen radicum onto a phylogenetic tree, they show it is present not only in orchids, but throughout the monocotyledons (in 74 genera from 22 monocot non-orchid families). Their conclusion is that monocots are highly flexible in allowing a transition from a persistent rhizodermis to the specialized velamen radicum, so it can reappear in diverse genera. Zotz et al. (2017) also discuss multiple functions ascribed to the velamen with respect to water and nutrients in epiphytic orchids, writing, ‘unfortunately, the experimental evidence for most of these functions is sketchy or missing entirely’, and including discussion of the controversial concept of it being a ‘pre adaptation’. Clearly, there is both a need for more comprehensive study of the occurrence (not least in roots of all orchids) and function of this unusual root adaptation.
Although unrelated to the orchids, carnivorous plants in genus Utricularia (Lentibulariaceae) are known as the ‘orchid-like bladderworts’, because of the crested corolla on their flowers. Gomes Rodrigues et al. (2017) show that the crested corolla has appeared at least twice during their phylogeny, before loss and then reversion in another lineage. By combining study of the morphological adaptations with molecular markers, the authors show that two infrageneric taxa are not monophyletic and should be combined. The tubers of this group, an adaptation for water storage, have been derived at least twice from stolons, being lost again in one lineage.
In the second manuscript on Utricularia species in this Special Issue, Płachno et al. (2017) reveal a unique structure in the genus – tubular extensions from the nucleus filled with chromatin, named chromatubules. These provide an excellent example of a novel structure that seems to be a recent evolutionary innovation. The authors speculate on its involvement in nucleus to cell to cell communication, although more research will be needed to define any functions.
Teisher et al. (2017) focus on phylogeny and morphological adaptations in one of the best-studied families, the Poaceae, showing that significant issues are found not only in unusual families like Lentibulariaceae (see above). They developed a large-scale dataset of complete plastome sequences from 107 genera across all grass sub-families, studying a conspicuous floral character of the twisted geniculate lemma awn. Anatomical characters were examined in more detail in the particular target species of their study that generally might be placed in the subfamily Arundionoideae. The DNA phylogeny showed the former circumscription of the subfamily was polyphyletic, and the authors present a new and robust picture of the relationships of the grass genera. The twisted geniculate awn, an ecologically important trait for seed germination, has arisen no less than five times in three subfamilies, highlighting the convergent and parallel evolution in the grass family.
REPRODUCTIVE TRAIT MORPHOLOGY
Reproductive traits are some of those which show the greatest variation in plant morphology. Among the greatest pioneers of botany, flowers were the key character used by Linneaus in enabling related plants to be grouped, while Charles Darwin examined many aspects of pollination, not least heterostyly discussed by Yuan et al. (2017). Following the transition to flowering at the shoot apical meristem (SAM), the developmental biology of floral organization and architecture is becoming well understood (Fernández-Mazuecos and Glover 2017), and the work by Jeiter et al. (2017) examines a specific component of floral organization: the nectaries. In Geraniaceae and Hypseocharitaceae, they can show an evolutionary series where nectaries have broad diversity despite the superficial simplicity and similarity of the flowers as a functional system in these families.
Plant-pollinator interactions and co-evolution have been widely considered (not least in previous Special Issues of Annals of Botany, included in consideration of Developmental Robustness and Species Diversity, Theissen and Metzer, 2016; and Pollinator-Driven speciation, van der Niet et al. 2014). Plants must go to great lengths to avoid damage and feeding animals where the plant gains no benefit – this leads to frequent morphological adaptations such as spines or biochemical irritants or poisons. But many plants must also attract animals for purposes such as pollination and seed dispersal. Luo et al. (2017) consider a particular plant product, resin, that acts in both capacities as herbivore defence and floral reward. They show that co-evolution of floral structures with nocturnal pollinating resin midges has led to resin-covered nurseries in remarkably species-specific mutualisms that have evolved in a few million years in the primitive Schisandraceae family. Aranda-Rickert et al. (2017) considers sugar exudates from wasp galls, concluding they are not analogous to the extrafloral nectary, but a facultative mutualism between the plant and several species, with particular advantages to the gall wasps.
Three further papers explore floral features and pollination, relating morphology and adaptation, with implications for evolution and phylogeny. Thaowetsuwan et al. (2017) study cellular and sub-cellular anatomy of species in the Sabiaceae, revealing the primitive and derived characters with a secondary pollen presentation adapting to pollination by small insects. Sapir et al. (2017) discuss a plant adaptation that has been shown to make pollination more efficient: the anther position in wild radish. This study compared plants with different stamen lengths and anther exsertion, showing that these characters not only affect pollen deposition on the pollinator, but also fly visits per flower. The careful observations demonstrate the multiple ecological consequences of changes in floral traits, something that must be considered in studies and has potential impact for plant fertility in a crop context.
Heterostyly is an adaptation found in numerous families that enables outbreeding in dioecious flowers, complementing self-incompatibility mechanisms. However, an evolutionary transition to homostyly with high levels of self-fertilization is frequently seen, with consequences for the genetic structure, evolution and adaptation of the species. These are found in population studies and can be understood with theoretical modelling. Yuan et al. (2017) formulate three critical questions about ecological correlates and genetic consequences of evolutionary transitions from distyly to homostyly. They address these questions using 14 populations of Primula oreodoxa, finding that homostyles set more seeds than distylous morphs following open pollination, although there are fewer long-tongued pollinator visits. Despite the lower genetic diversity in the homostylous populations, these populations benefited from reproductive certainty through self-pollination allowed by loss of heterostyly.
ADAPTATION AND ECOLOGY
All of the papers in this special issue have ecological implications arising from the morphological features that are discussed. But two papers relate more specifically to adaptation in an ecological or environmental context. Mosses, growing on the soil surface, play an important role in hydrology and nutrient cycling in many, particularly temperate, ecosystems, as pointed out by Sokolowska et al. (2017). By examining the stem anatomy in two feather mosses, and using fluorescent tracers, they were able to show the nature of internal, symplastic, and apoplastic transport, showing also the changes with air humidity. The combination of morphological, experimental and comparative studies of species from two genera enable the authors to consider why one species dries out more than the other, the adaptations to stabilize water content, and consequently the role of the mosses in drier and wetter ecosystems with respect to water and nutrient cycling.
Qian et al. (2017) tackle an ecologically important adaptation of bud-banks: the energetically costly bud-bearing organs below ground. They compare multiple environments across 21 sites, with variation in precipitation, and temperature, showing bud bank density is lower in hot environments with water also playing a part. Tussock grasses have more resistant bud types than rhizomatous species. These adaptive strategies enabling regeneration and lateral spread of species have clear implications for choice in protecting water catchments from erosion, and in the future for ecosystem evolution under changing climates.
CONCLUSIONS
The articles in this special issue include studies of a diverse range of species from many ecosystems, using the full range of techniques available to the botanist. All the papers discuss fundamental research, with largely non-crop species, but the implications for both crop production and ecosystem or environmental conservation are apparent in all. As genes involved in morphology become more widely understood, we can improve outcomes and consider what is needed from crops – the superdomestication concept, deciding what is needed and then looking for the source of genes to deliver that requirement (considered in another Special Issue on Domestication, Vaughan et al., 2007). Domestication genes may become a potent area of interest for future morphological adaptations: perhaps increasing the number of species where it is worthwhile to farm them.
Annals of Botany includes a ‘Snapshot’ for each paper in the front of each issues. These are written by the authors (but may be edited by the Editors), and aim to bring out the importance of the manuscript in its field in a less formal way than the scientific abstracts of the articles. I was reading all these Snapshots (pp. i-iv) while finalizing this Preface for our Morphology and Adaptation Special Issue. It was interesting to find that concentrating on the overarching theme of morphology and adaptation, I had often highlighted different aspects and implications of the work to those the authors choose to focus on, both in their Snapshot and the whole article. In bringing out the relevance of the research to our topic of Morphology and Adaptation, I hope the Special Issue grouping will encourage readers and researchers to think about the impact of this broad range of research from a different angle.
