"Plant biology" redirects here. For other uses, see Botany (disambiguation) and Botanic.
Botany, also called plant science(s), plant biology or phytology, is the science of plant life and a branch of biology. A botanist, plant scientist or phytologist is a scientist who specialises in this field. The term "botany" comes from the Ancient Greek word βοτάνη (botanē) meaning "pasture", "grass", or "fodder"; βοτάνη is in turn derived from βόσκειν (boskein), "to feed" or "to graze". Traditionally, botany has also included the study of fungi and algae by mycologists and phycologists respectively, with the study of these three groups of organisms remaining within the sphere of interest of the International Botanical Congress. Nowadays, botanists (in the strict sense) study approximately 410,000 species of land plants of which some 391,000 species are vascular plants (including ca 369,000 species of flowering plants), and ca 20,000 are bryophytes.
Botany originated in prehistory as herbalism with the efforts of early humans to identify – and later cultivate – edible, medicinal and poisonous plants, making it one of the oldest branches of science. Medieval physic gardens, often attached to monasteries, contained plants of medical importance. They were forerunners of the first botanical gardens attached to universities, founded from the 1540s onwards. One of the earliest was the Padua botanical garden. These gardens facilitated the academic study of plants. Efforts to catalogue and describe their collections were the beginnings of plant taxonomy, and led in 1753 to the binomial system of Carl Linnaeus that remains in use to this day.
In the 19th and 20th centuries, new techniques were developed for the study of plants, including methods of optical microscopy and live cell imaging, electron microscopy, analysis of chromosome number, plant chemistry and the structure and function of enzymes and other proteins. In the last two decades of the 20th century, botanists exploited the techniques of molecular genetic analysis, including genomics and proteomics and DNA sequences to classify plants more accurately.
Modern botany is a broad, multidisciplinary subject with inputs from most other areas of science and technology. Research topics include the study of plant structure, growth and differentiation, reproduction, biochemistry and primary metabolism, chemical products, development, diseases, evolutionary relationships, systematics, and plant taxonomy. Dominant themes in 21st century plant science are molecular genetics and epigenetics, which are the mechanisms and control of gene expression during differentiation of plant cells and tissues. Botanical research has diverse applications in providing staple foods, materials such as timber, oil, rubber, fibre and drugs, in modern horticulture, agriculture and forestry, plant propagation, breeding and genetic modification, in the synthesis of chemicals and raw materials for construction and energy production, in environmental management, and the maintenance of biodiversity.
Main article: History of botany
Botany originated as herbalism, the study and use of plants for their medicinal properties. Many records of the Holocene period date early botanical knowledge as far back as 10,000 years ago. This early unrecorded knowledge of plants was discovered in ancient sites of human occupation within Tennessee, which make up much of the Cherokee land today. The early recorded history of botany includes many ancient writings and plant classifications. Examples of early botanical works have been found in ancient texts from India dating back to before 1100 BC, in archaic Avestan writings, and in works from China before it was unified in 221 BC.
Modern botany traces its roots back to Ancient Greece specifically to Theophrastus (c. 371–287 BC), a student of Aristotle who invented and described many of its principles and is widely regarded in the scientific community as the "Father of Botany". His major works, Enquiry into Plants and On the Causes of Plants, constitute the most important contributions to botanical science until the Middle Ages, almost seventeen centuries later.
Another work from Ancient Greece that made an early impact on botany is De Materia Medica, a five-volume encyclopedia about herbal medicine written in the middle of the first century by Greek physician and pharmacologist Pedanius Dioscorides. De Materia Medica was widely read for more than 1,500 years. Important contributions from the medieval Muslim world include Ibn Wahshiyya's Nabatean Agriculture, Abū Ḥanīfa Dīnawarī's (828–896) the Book of Plants, and Ibn Bassal's The Classification of Soils. In the early 13th century, Abu al-Abbas al-Nabati, and Ibn al-Baitar (d. 1248) wrote on botany in a systematic and scientific manner.
In the mid-16th century, "botanical gardens" were founded in a number of Italian universities – the Padua botanical garden in 1545 is usually considered to be the first which is still in its original location. These gardens continued the practical value of earlier "physic gardens", often associated with monasteries, in which plants were cultivated for medical use. They supported the growth of botany as an academic subject. Lectures were given about the plants grown in the gardens and their medical uses demonstrated. Botanical gardens came much later to northern Europe; the first in England was the University of Oxford Botanic Garden in 1621. Throughout this period, botany remained firmly subordinate to medicine.
German physician Leonhart Fuchs (1501–1566) was one of "the three German fathers of botany", along with theologian Otto Brunfels (1489–1534) and physician Hieronymus Bock (1498–1554) (also called Hieronymus Tragus). Fuchs and Brunfels broke away from the tradition of copying earlier works to make original observations of their own. Bock created his own system of plant classification.
Physician Valerius Cordus (1515–1544) authored a botanically and pharmacologically important herbal Historia Plantarum in 1544 and a pharmacopoeia of lasting importance, the Dispensatorium in 1546. Naturalist Conrad von Gesner (1516–1565) and herbalist John Gerard (1545–c. 1611) published herbals covering the medicinal uses of plants. Naturalist Ulisse Aldrovandi (1522–1605) was considered the father of natural history, which included the study of plants. In 1665, using an early microscope, PolymathRobert Hooke discovered cells, a term he coined, in cork, and a short time later in living plant tissue.
Early modern botany
Further information: Taxonomy (biology) § History of taxonomy
During the 18th century, systems of plant identification were developed comparable to dichotomous keys, where unidentified plants are placed into taxonomic groups (e.g. family, genus and species) by making a series of choices between pairs of characters. The choice and sequence of the characters may be artificial in keys designed purely for identification (diagnostic keys) or more closely related to the natural or phyletic order of the taxa in synoptic keys. By the 18th century, new plants for study were arriving in Europe in increasing numbers from newly discovered countries and the European colonies worldwide. In 1753 Carl von Linné (Carl Linnaeus) published his Species Plantarum, a hierarchical classification of plant species that remains the reference point for modern botanical nomenclature. This established a standardised binomial or two-part naming scheme where the first name represented the genus and the second identified the species within the genus. For the purposes of identification, Linnaeus's Systema Sexualeclassified plants into 24 groups according to the number of their male sexual organs. The 24th group, Cryptogamia, included all plants with concealed reproductive parts, mosses, liverworts, ferns, algae and fungi.
Increasing knowledge of plant anatomy, morphology and life cycles led to the realisation that there were more natural affinities between plants than the artificial sexual system of Linnaeus. Adanson (1763), de Jussieu (1789), and Candolle (1819) all proposed various alternative natural systems of classification that grouped plants using a wider range of shared characters and were widely followed. The Candollean system reflected his ideas of the progression of morphological complexity and the later classification by Bentham and Hooker, which was influential until the mid-19th century, was influenced by Candolle's approach. Darwin's publication of the Origin of Species in 1859 and his concept of common descent required modifications to the Candollean system to reflect evolutionary relationships as distinct from mere morphological similarity.
Botany was greatly stimulated by the appearance of the first "modern" textbook, Matthias Schleiden's Grundzüge der Wissenschaftlichen Botanik, published in English in 1849 as Principles of Scientific Botany. Schleiden was a microscopist and an early plant anatomist who co-founded the cell theory with Theodor Schwann and Rudolf Virchow and was among the first to grasp the significance of the cell nucleus that had been described by Robert Brown in 1831. In 1855, Adolf Fick formulated Fick's laws that enabled the calculation of the rates of molecular diffusion in biological systems.
Late modern botany
Building upon the gene-chromosome theory of heredity that originated with Gregor Mendel (1822–1884), August Weismann (1834–1914) proved that inheritance only takes place through gametes. No other cells can pass on inherited characters. The work of Katherine Esau (1898–1997) on plant anatomy is still a major foundation of modern botany. Her books Plant Anatomy and Anatomy of Seed Plants have been key plant structural biology texts for more than half a century.
The discipline of plant ecology was pioneered in the late 19th century by botanists such as Eugenius Warming, who produced the hypothesis that plants form communities, and his mentor and successor Christen C. Raunkiær whose system for describing plant life forms is still in use today. The concept that the composition of plant communities such as temperate broadleaf forest changes by a process of ecological succession was developed by Henry Chandler Cowles, Arthur Tansley and Frederic Clements. Clements is credited with the idea of climax vegetation as the most complex vegetation that an environment can support and Tansley introduced the concept of ecosystems to biology. Building on the extensive earlier work of Alphonse de Candolle, Nikolai Vavilov (1887–1943) produced accounts of the biogeography, centres of origin, and evolutionary history of economic plants.
Particularly since the mid-1960s there have been advances in understanding of the physics of plant physiological processes such as transpiration (the transport of water within plant tissues), the temperature dependence of rates of water evaporation from the leaf surface and the molecular diffusion of water vapour and carbon dioxide through stomatal apertures. These developments, coupled with new methods for measuring the size of stomatal apertures, and the rate of photosynthesis have enabled precise description of the rates of gas exchange between plants and the atmosphere. Innovations in statistical analysis by Ronald Fisher,Frank Yates and others at Rothamsted Experimental Station facilitated rational experimental design and data analysis in botanical research. The discovery and identification of the auxinplant hormones by Kenneth V. Thimann in 1948 enabled regulation of plant growth by externally applied chemicals. Frederick Campion Steward pioneered techniques of micropropagation and plant tissue culture controlled by plant hormones. The synthetic auxin 2,4-Dichlorophenoxyacetic acid or 2,4-D was one of the first commercial synthetic herbicides.
20th century developments in plant biochemistry have been driven by modern techniques of organic chemical analysis, such as spectroscopy, chromatography and electrophoresis. With the rise of the related molecular-scale biological approaches of molecular biology, genomics, proteomics and metabolomics, the relationship between the plant genome and most aspects of the biochemistry, physiology, morphology and behaviour of plants can be subjected to detailed experimental analysis. The concept originally stated by Gottlieb Haberlandt in 1902 that all plant cells are totipotent and can be grown in vitro ultimately enabled the use of genetic engineering experimentally to knock out a gene or genes responsible for a specific trait, or to add genes such as GFP that report when a gene of interest is being expressed. These technologies enable the biotechnological use of whole plants or plant cell cultures grown in bioreactors to synthesise pesticides, antibiotics or other pharmaceuticals, as well as the practical application of genetically modified crops designed for traits such as improved yield.
Modern morphology recognises a continuum between the major morphological categories of root, stem (caulome), leaf (phyllome) and trichome. Furthermore, it emphasises structural dynamics. Modern systematics aims to reflect and discover phylogenetic relationships between plants. Modern Molecular phylogenetics largely ignores morphological characters, relying on DNA sequences as data. Molecular analysis of DNA sequences from most families of flowering plants enabled the Angiosperm Phylogeny Group to publish in 1998 a phylogeny of flowering plants, answering many of the questions about relationships among angiosperm families and species. The theoretical possibility of a practical method for identification of plant species and commercial varieties by DNA barcoding is the subject of active current research.
Scope and importance
The study of plants is vital because they underpin almost all animal life on Earth by generating a large proportion of the oxygen and food that provide humans and other organisms with aerobic respiration with the chemical energy they need to exist. Plants, algae and cyanobacteria are the major groups of organisms that carry out photosynthesis, a process that uses the energy of sunlight to convert water and carbon dioxide into sugars that can be used both as a source of chemical energy and of organic molecules that are used in the structural components of cells. As a by-product of photosynthesis, plants release oxygen into the atmosphere, a gas that is required by nearly all living things to carry out cellular respiration. In addition, they are influential in the global carbon and water cycles and plant roots bind and stabilise soils, preventing soil erosion. Plants are crucial to the future of human society as they provide food, oxygen, medicine, and products for people, as well as creating and preserving soil.
Historically, all living things were classified as either animals or plants and botany covered the study of all organisms not considered animals. Botanists examine both the internal functions and processes within plant organelles, cells, tissues, whole plants, plant populations and plant communities. At each of these levels, a botanist may be concerned with the classification (taxonomy), phylogeny and evolution, structure (anatomy and morphology), or function (physiology) of plant life.
The strictest definition of "plant" includes only the "land plants" or embryophytes, which include seed plants (gymnosperms, including the pines, and flowering plants) and the free-sporing cryptogams including ferns, clubmosses, liverworts, hornworts and mosses. Embryophytes are multicellular eukaryotes descended from an ancestor that obtained its energy from sunlight by photosynthesis. They have life cycles with alternatinghaploid and diploid phases. The sexual haploid phase of embryophytes, known as the gametophyte, nurtures the developing diploid embryo sporophyte within its tissues for at least part of its life, even in the seed plants, where the gametophyte itself is nurtured by its parent sporophyte. Other groups of organisms that were previously studied by botanists include bacteria (now studied in bacteriology), fungi (mycology) – including lichen-forming fungi (lichenology), non-chlorophytealgae (phycology), and viruses (virology). However, attention is still given to these groups by botanists, and fungi (including lichens) and photosynthetic protists are usually covered in introductory botany courses.
Palaeobotanists study ancient plants in the fossil record to provide information about the evolutionary history of plants. Cyanobacteria, the first oxygen-releasing photosynthetic organisms on Earth, are thought to have given rise to the ancestor of plants by entering into an endosymbiotic relationship with an early eukaryote, ultimately becoming the chloroplasts in plant cells. The new photosynthetic plants (along with their algal relatives) accelerated the rise in atmospheric oxygen started by the cyanobacteria, changing the ancient oxygen-free, reducing, atmosphere to one in which free oxygen has been abundant for more than 2 billion years.
Among the important botanical questions of the 21st century are the role of plants as primary producers in the global cycling of life's basic ingredients: energy, carbon, oxygen, nitrogen and water, and ways that our plant stewardship can help address the global environmental issues of resource management, conservation, human food security, biologically invasive organisms, carbon sequestration, climate change, and sustainability.
Further information: Human nutrition
Virtually all staple foods come either directly from primary production by plants, or indirectly from animals that eat them. Plants and other photosynthetic organisms are at the base of most food chains because they use the energy from the sun and nutrients from the soil and atmosphere, converting them into a form that can be used by animals. This is what ecologists call the first trophic level. The modern forms of the major staple foods, such as maize, rice, wheat and other cereal grasses, pulses, bananas and plantains, as well as flax and cotton grown for their fibres, are the outcome of prehistoric selection over thousands of years from among wild ancestral plants with the most desirable characteristics.
Botanists study how plants produce food and how to increase yields, for example through plant breeding, making their work important to mankind's ability to feed the world and provide food security for future generations. Botanists also study weeds, which are a considerable problem in agriculture, and the biology and control of plant pathogens in agriculture and natural ecosystems.Ethnobotany is the study of the relationships between plants and people. When applied to the investigation of historical plant–people relationships ethnobotany may be referred to as archaeobotany or palaeoethnobotany. Some of the earliest plant-people relationships arose between the indigenous people of Canada in identifying edible plants from inedible plants. This relationship the indigenous people had with plants was recorded by ethnobotanists.
Plant biochemistry is the study of the chemical processes used by plants. Some of these processes are used in their primary metabolism like the photosynthetic Calvin cycle and crassulacean acid metabolism. Others make specialised materials like the cellulose and lignin used to build their bodies, and secondary products like resins and aroma compounds.
Plants and various other groups of photosynthetic eukaryotes collectively known as "algae" have unique organelles known as chloroplasts. Chloroplasts are thought to be descended from cyanobacteria that formed endosymbiotic relationships with ancient plant and algal ancestors. Chloroplasts and cyanobacteria contain the blue-green pigment chlorophyll a. Chlorophyll a (as well as its plant and green algal-specific cousin chlorophyll b)[a] absorbs light in the blue-violet and orange/red parts of the spectrum while reflecting and transmitting the green light that we see as the characteristic colour of these organisms. The energy in the red and blue light that these pigments absorb is used by chloroplasts to make energy-rich carbon compounds from carbon dioxide and water by oxygenic photosynthesis, a process that generates molecular oxygen (O2) as a by-product.
The light energy captured by chlorophyll a is initially in the form of electrons (and later a proton gradient) that's used to make molecules of ATP and NADPH which temporarily store and transport energy. Their energy is used in the light-independent reactions of the Calvin cycle by the enzyme rubisco to produce molecules of the 3-carbon sugar glyceraldehyde 3-phosphate (G3P). Glyceraldehyde 3-phosphate is the first product of photosynthesis and the raw material from which glucose and almost all other organic molecules of biological origin are synthesised. Some of the glucose is converted to starch which is stored in the chloroplast. Starch is the characteristic energy store of most land plants and algae, while inulin, a polymer of fructose is used for the same purpose in the sunflower family Asteraceae. Some of the glucose is converted to sucrose (common table sugar) for export to the rest of the plant.
Unlike in animals (which lack chloroplasts), plants and their eukaryote relatives have delegated many biochemical roles to their chloroplasts, including synthesising all their fatty acids, and most amino acids. The fatty acids that chloroplasts make are used for many things, such as providing material to build cell membranes out of and making the polymer cutin which is found in the plant cuticle that protects land plants from drying out.
Plants synthesise a number of unique polymers like the polysaccharide molecules cellulose, pectin and xyloglucan from which the land plant cell wall is constructed. Vascular land plants make lignin, a polymer used to strengthen the secondary cell walls of xylem tracheids and vessels to keep them from collapsing when a plant sucks water through them under water stress. Lignin is also used in other cell types like sclerenchyma fibres that provide structural support for a plant and is a major constituent of wood. Sporopollenin is a chemically resistant polymer found in the outer cell walls of spores and pollen of land plants responsible for the survival of early land plant spores and the pollen of seed plants in the fossil record. It is widely regarded as a marker for the start of land plant evolution during the Ordovician period. The concentration of carbon dioxide in the atmosphere today is much lower than it was when plants emerged onto land during the Ordovician and Silurian periods. Many monocots like maize and the pineapple and some dicots like the Asteraceae have since independently evolved pathways like Crassulacean acid metabolism and the C4 carbon fixation pathway for photosynthesis which avoid the losses resulting from photorespiration in the more common C3 carbon fixation pathway. These biochemical strategies are unique to land plants.
Medicine and materials
Phytochemistry is a branch of plant biochemistry primarily concerned with the chemical substances produced by plants during secondary metabolism. Some of these compounds are toxins such as the alkaloidconiine from hemlock. Others, such as the essential oilspeppermint oil and lemon oil are useful for their aroma, as flavourings and spices (e.g., capsaicin), and in medicine as pharmaceuticals as in opium from opium poppies. Many medicinal and recreational drugs, such as tetrahydrocannabinol (active ingredient in cannabis), caffeine, morphine and nicotine come directly from plants. Others are simple derivatives of botanical natural products. For example, the pain killer aspirin is the acetyl ester of salicylic acid, originally isolated from the bark of willow trees, and a wide range of opiatepainkillers like heroin are obtained by chemical modification of morphine obtained from the opium poppy. Popular stimulants come from plants, such as caffeine from coffee, tea and chocolate, and nicotine from tobacco. Most alcoholic beverages come from fermentation of carbohydrate-rich plant products such as barley (beer), rice (sake) and grapes (wine).Native Americans have used various plants as ways of treating illness or disease for thousands of years. This knowledge Native Americans have on plants has been recorded by enthnobotanists and then in turn has been used by pharmaceutical companies as a way of drug discovery.
Plants can synthesise useful coloured dyes and pigments such as the anthocyanins responsible for the red colour of red wine, yellow weld and blue woad used together to produce Lincoln green, indoxyl, source of the blue dye indigo traditionally used to dye denim and the artist's pigments gamboge and rose madder. Sugar, starch, cotton, linen, hemp, some types of rope, wood and particle boards, papyrus and paper, vegetable oils, wax, and natural rubber are examples of commercially important materials made from plant tissues or their secondary products. Charcoal, a pure form of carbon made by pyrolysis of wood, has a long history as a metal-smelting fuel, as a filter material and adsorbent and as an artist's material and is one of the three ingredients of gunpowder. Cellulose, the world's most abundant organic polymer, can be converted into energy, fuels, materials and chemical feedstock. Products made from cellulose include rayon and cellophane, wallpaper paste, biobutanol and gun cotton. Sugarcane, rapeseed and soy are some of the plants with a highly fermentable sugar or oil content that are used as sources of biofuels, important alternatives to fossil fuels, such as biodiesel. Sweetgrass was used by NativeAmericanse to ward of bugs like mosquitoes. These bug repelling properties of sweetgrass were later found by the American Chemical Society in the molecules phytol and coumarin.
Main article: Plant ecology
Plant ecology is the science of the functional relationships between plants and their habitats—the environments where they complete their life cycles. Plant ecologists study the composition of local and regional floras, their biodiversity, genetic diversity and fitness, the adaptation of plants to their environment, and their competitive or mutualistic interactions with other species. Some ecologists even rely on empirical data from indigenous people that is gathered by ethnobotanists. This information can relay a great deal of information on how the land once was thousands of years ago and how it has changed over that time. The goals of plant ecology are to understand the causes of their distribution patterns, productivity, environmental impact, evolution, and responses to environmental change.
Plants depend on certain edaphic (soil) and climatic factors in their environment but can modify these factors too. For example, they can change their environment's albedo, increase runoff interception, stabilise mineral soils and develop their organic content, and affect local temperature. Plants compete with other organisms in their ecosystem for resources. They interact with their neighbours at a variety of spatial scales
The Calvin cycle(Interactive diagram) The Calvin cycle incorporates carbon dioxide into sugar molecules.
Living botanical collections include germplasm repositories, long-term experimental plantings, and botanical gardens. We present here a series of vignettes to illustrate the central role that living collections have played in plant biology research, including evo-devo research. Looking toward the future, living collections will become increasingly important in support of future evo-devo research. The driving force behind this trend is nucleic acid sequencing technologies, which are rapidly becoming more powerful and cost-effective, and which can be applied to virtually any species. This allows for more extensive sampling, including non-model organisms with unique biological features and plants from diverse phylogenetic positions. Importantly, a major challenge for sequencing-based evo-devo research is to identify, access, and propagate appropriate plant materials. We use a vignette of the ongoing 1,000 Transcriptomes project as an example of the challenges faced by such projects. We conclude by identifying some of the pinch points likely to be encountered by future evo-devo researchers, and how living collections can help address them.
Keywords: botanical gardens, genomics, plant developmental biology, next generation sequencing, outreach
INTRODUCTION: LIVING BOTANICAL COLLECTIONS IN HISTORICAL CONTEXT
Living collections are curated for various purposes including scientific education and research. For plants, living collections include germplasm repositories – such as the world’s largest, the National Plant Germplasm System (NPGS) of USDA – that preserve plant genetic resources for research and conservation. There are also experimental research plots, seed banks, conservatories, and germplasm repositories for research that are associated with universities and research institutions. Lastly, there are the public facing botanical gardens – some 3,000 worldwide according to Botanic Gardens Conservation International. Although their raison d’être is assumed by some to be display and education, their living collections also serve vital research roles.
The earliest gardens (e.g., Padua, founded in 1545) served the apothecary and physician, but during the subsequent age of exploration, these collections grew to become living encyclopedias ripe for comparative and descriptive work. With botany and taxonomy as driving forces, scholars used these cultivated plants to describe, name, and place these species into ordered groups. Over time, some gardens diversified, while others specialized. For instance, the Palm House at the Royal Botanic Gardens, Kew, opened in 1848 and provided this institution of diverse yet temperate plants the opportunity to cultivate and study a broader range of tropical plants collected by explorer scientists. While comprehensive or general collections such as Kew and the Missouri Botanical Garden thrived and multiplied, others focused their collections. For example, in 1872, the Arnold Arboretum of Harvard University became the first public botanical garden in the US to specialize in temperate woody plants. Other institutions defined the scope of their collections geographically, such as Rancho Santa Ana Botanic Garden, founded in 1927, which has botanical collections which represent the flora of California. The resulting impressive array of botanical resources began and continue to serve scientific disciplines beyond basic taxonomy and botany, including horticulture, plant breeding, conservation, and ecology.
LIVING COLLECTIONS FACILITATE PLANT BIOLOGY RESEARCH
Living collections have played diverse yet crucial roles in plant biology research. In general, identifying, acquiring, propagating, and growing appropriate plant materials are fundamental needs of almost all plant biology, and living collections are well positioned to meet these needs. This is especially true for evolution of development (evo-devo) research, which seeks to understand both the evolutionary history and molecular mechanisms underlying development and biological processes. Evo-devo research is defined by comparative approaches that require the ability to sample different ecotypes or species of interests.
The vignettes presented below illustrate the importance of living collections in plant biology research, ranging from applied research for plant breeding to evo-devo research – all of which hinged on the use of living collections. The need for access to plant materials is quickly becoming more acute as genomics-based evo-devo studies expand to encompass broader taxonomic groups and larger numbers of species. The final vignette of the 1,000 Transcriptomes Project (1KP) is used to illustrate some of the challenges and opportunities for living collections in a new age of genomics-based evo-devo.
MR. EDDY’S TREE BREEDING STATION AND ADAPTIVE TRAITS OF FOREST TREES
James G. Eddy was a lumberman from the Pacific Northwest who made a fortune from forest industry in the late 1800s. Realizing that forests were being cut at a rate far exceeding replacement, Eddy proposed that forest trees could be bred to produce superior performing stocks to make up the difference. In 1925, he established a tree breeding station located at Placerville, California. Lloyd Austin was hired as the first director of the Eddy Tree Breeding Station (now known as the Institute of Forest Genetics), and quickly set about establishing an extensive arboretum of conifers.
Around the same time, researchers Clausen, Keck, and Hiesey of Stanford established that herbaceous plants showed heritable traits associated with their local environments and elevations in the east to west environmental clines of California (Clausen et al., 1941). In general, seed collected and grown from plants at their native elevations performed better than seed collected from plants of the same species at higher or lower elevations. Realizing that similar effects could have significant impacts on reforestation efforts, Austin established an elevational gradient experiment for Pinus ponderosa and P. jeffreyi. Seed were collected from trees at different elevations, and then planted in three common planting sites ranging from low to high elevation. The significance of this experiment is presaged by correspondence from Hiesey to Austin after his visit to the Institute in 1938, in which he writes “The practical application to plant breeding are obvious, and for this reason I think your plan of starting a series of transect gardens is not only basically sound, but indispensable to realizing your objective to produce the best possible races for each climatic region.”
The long-term survival and performance of the Eddy Arboretum trees was only revealed after many decades, however, and the ranking of performance for families from different elevations changed during the course of long-term growth of the plantations (Namkoong and Conkle, 1976). Only after exposure to the full range of environmental challenges (e.g., harsh winters) over many years was it revealed that higher elevation seed sources ultimately performed better at high elevation sites than did lower elevation seed sources (Conkle, 1973). This research fully established the hereditary nature of adaptation for tree species, and was the basis of “seed zones” for reforestation.
DOMESTICATION, DETERMINACY, AND THE PHASEOLUS WORLD COLLECTION
Understanding the process of domestication provides important insight into the origins of crops and gives information about wild relatives vital to plant breeding efforts. While wild relatives can be important sources of unique alleles conferring disease resistance and other useful traits for agriculture, understanding the processes of domestication can also provide insight into the evolution of developmental traits as driven by human selection. One such example is given by Phaseolus, the genus containing the common bean (P. vulgaris).
One immediate challenge of studying domestication syndromes is acquiring germplasm representative of both domesticated varieties as well as wild relatives. Paul Gepts and colleagues wanted to understand the process by which domestication occurred independently in two geographic regions, giving rise to a Mesoamerican gene pool and an Andean gene pool within modern P. vulgaris varieties. Crucial to this research was the Phaseolus World Collection at CIAT, Cali, Colombia, as well as the collection maintained at the NPGS station in Pullman, Washington. Phylogenetic analysis of samples representing 100 wild and 249 domesticated cultivars revealed nine populations, four each of Andean and Mesoamerican origins, and one consisting of the likely wild ancestor of P. vulgaris (Kwak and Gepts, 2009; Kwak et al., 2009).
Related research investigated the genetic basis underlying the two major traits selected in Phaseolus domestication: photoperiod insensitivity and determinate growth habit. Plants with these traits can be grown at varied latitudes, and produce more rapid and synchronous flowering and fruiting. A cross between parents of Andean and Mesoamerican origins yielded a genetic mapping population. Using this and an assay of variation for candidate genes affecting flowering time in Arabidopsis revealed that homologs of Terminal Flower 1 (TFL1) mapped to quantitative trait loci affecting determinacy (Kwak et al., 2008). This research shows the potential power of comparative approaches, and holds great promise for plant breeding applications.
A HAND-DRAWN PICTURE IS WORTH A 1000 WORDS: THE EUPOMATIACEAE OF ZURICH
It is hard to overemphasize the role of botanical gardens in providing researchers the ability to closely observe the growth and development of their subjects – to have “a feeling for the organism,” as Barbara McClintock put it (Keller, 1983). Throughout his career, Peter Endress’ access to living collections at the Botanic Garden of the University of Zurich has been essential to his study of floral development. In fact, his early impressions of Eupomatiaceae can be traced to his acute observations – including detailed hand drawings (Figure 1) – of flowering material in the 1970s. In an essay (Endress, 2008), he emphasized “the great heuristic value of drawings,” noting that “the process of hand drawing can provide valuable insights into patterns or processes of nature, which can scarcely be achieved by merely looking at and analyzing a picture taken by a camera or the SEM.” Subsequent studies (Endress, 2003; Kim et al., 2005) revealed and confirmed the nature of the unusual cap, or calyptra, which covers the floral organs during their development: it is a bract, not a modification of the perianth.
An opening flower of Eupomatia bennettii F. Muell., drawn by Peter Endress on 5 February 1979 at 09.00 h (A) and 14.00 h (B). The inner staminodes are shown bearing secretory warts during the male phase of anthesis (A), while the exposed gynoecium is...
CHARLIE RICK’S TOMATOES AND THE REGULATION OF LEAF COMPLEXITY
Charlie Rick devoted most of his long career as a botanist to the study of genetic variation in tomato (Solanum spp.), using pioneering cytological and genetic approaches. During the course of his research, he made multiple collecting expeditions to South America and the Galapagos Islands to sample the diversity found in wild species. Today, the C. M. Rick Tomato Genetics Resource Center at the University of California Davis has over 3,600 active accessions available for plant breeding and research.
Neelima Sinha has benefitted from Charlie Rick’s collections in the course of her research of leaf complexity. Neelima first met Charlie during her graduate studies at UC Berkeley. Interested in the mouse ears (Me) mutation that causes changes in the degree of leaf compoundedness, Neelima contacted Charlie, who not only granted her request for heterozygous Me seed for genetic mapping, but also included additional alleles and insight into Me phenotypes in other genetic backgrounds (N. Sinha, personal communication). Years later, Neelima acquired seed of Solanum cheesmaniae and S. galapagense through the Resource Center. Darwin first collected seed from these species, which were later characterized by J. G. Hooker for their differences in leaf compoundedness (Hooker, 1847). Neelima used them to map the causative locus to a gene, PETEROSELINUM (PTS), which encodes a novel KNOX transcription factor that lacks the homeodomain required for KNOX protein function (Kimura et al., 2008). Because KNOX proteins act as heterodimers, the PTS-encoded protein competes with legitimate KNOX proteins, which normally increase leaf compoundeness. PTS thus represents a novel mechanism by which leaf morphology is regulated through a naturally occurring mutation.
THE 1,000 TRANSCRIPTOMES PROJECT AND THE ORIGIN OF SAMPLES
Recent advances in sequencing technologies have greatly expanded the scope of evo-devo research (Rokas and Abbot, 2009). A bold example is the 1KP Project, a multi-institutional effort that is surveying gene expression in leaves (and for some species flowers or other tissues) from 1,000 green plant species1, In many regards, this project represents a paradigm shift in plant biology and in particular plant evo-devo research. Until recently, large sequencing projects were restricted to a modest number of well-developed model species. The rapidly decreasing cost and increasing output from “next generation” sequencing (Mardis, 2008; Schuster, 2008) now allows a different strategy, in which diverse species can be selected for study based on phylogenetic position and biological traits of interest. Sequencing the transcriptomes (as opposed to the genomes) of plants has a number of advantages (Wang et al., 2009). Transcriptomes are less complex and can be assembled de novo directly from sequence reads; they provide information about gene structure and alternative splicing; and they provide information about gene expression in the tissues sampled. Some of the broad objectives of 1KP include determining the relationship of gene expression in gametophyte-dominant versus sporophyte-dominant plants, identifying ancient polyploidization events in angiosperms, and testing for correlation between polyploidization and species richness. In addition, each transcriptome provides resources for the sequenced species, and also provides opportunities for comparative analyses across tissue types and taxa.
A number of practical issues associated with 1KP will be common to future genomic-based evo-devo studies. Obtaining appropriate plant materials from a diverse array of plant species is no small task. Some specimens were collected in the wild or from opportunistic locations including backyards – the accession for Oenothera grandiflora includes the GPS coordinates of the plant sampled and annotation to “ask the nice lady for permission to collect” at a home in Bigbee, Alabama. Field-based collections were made more challenging still because flash freezing of tissue samples using liquid nitrogen was found necessary to reliably preserve tissues for RNA isolation from the range of species sampled (D. Soltis, personal communication). Specimens from botanical gardens or other living collections are much preferred not just for ease of access, but because they have known provenance, additional collections can be made in the future, and the plants can be observed, propagated, or potentially experimentally manipulated. In addition, gene expression can be affected by a wide variety of factors ranging from environmental to genetic to developmental stage. To make comparisons in gene expression between, say, leaves of two species, it will often be desirable to have the plants for comparison grown under similar conditions and collected at the same time and growth stage. Living collections and botanical gardens in particular are well positioned to provide such materials, and 1KP benefitted from principal investigators and collaborators associated with institutions including the New York Botanical Garden, Kew, and the University of British Columbia Botanical Garden and Centre for Plant Research.
LIVING COLLECTIONS FACILITATE GENOMICS-BASED EVO-DEVO RESEARCH
While genomic and next generation sequencing approaches are well suited for evo-devo research, they alone are insufficient. Indeed, a major challenge of plant evo-devo research is to develop an initial understanding of the trait through direct observation, then assembling plant materials representing a range of taxonomic and phenotypic variation for the trait, and finally quantifying variation in that trait across taxa. This is a significant challenge when one considers the breadth of plant biodiversity, the near limitless traits to study, and the range of environments within which they occur. Fortunately, genomics researchers have direct access to the extensive range of living plant collections. Collectively, these living libraries possess a rich array of well-documented plant materials maintained by knowledgeable curatorial and horticultural staff, and are available for research and discovery.
Collections not only comprise wild-provenance material that may be challenging to obtain, but also artificial hybrids of known pedigree, and ornamental variants selected for their horticultural value that would only be recognized and able to thrive under contrived conditions. This latter group serves as a unique resource for evo-devo investigation, and contains a wealth of genetic diversity including chimeras and spontaneously arising mutants (Dosmann, 2006). The research potential of atypical forms or mutants growing but meters away from their wild-type cousins is compelling. And, because many identical cultivars as well as accessions of known wild provenance are replicated in collections around the world, it is possible to examine variability as a function of environment. It is striking that living collections also serve as repositories for future research, particularly in underdeveloped and unforeseen areas (Tanksley and McCouch, 1997; Dosmann, 2006; Donaldson, 2009). In the example presented above of the Eddy Arboretum, those trees have experienced much of the industrial age of global climate change and contain a record of their growth in the form of annual rings. They therefore represent a valuable resource for measuring the response of different genotypes to environmental change, which was unforeseen at the time of their planting.
Another important distinction among these collections is the fact that they can be well documented with data such as provenance, verification status, morphological measurements, previous research results, as well as voucher herbarium specimens and images. They are also curated by experts in systematics, horticulture, plant anatomy and morphology, and other disciplines. In fact, the horticultural and curatorial staff not only preserve, study, and document these collections, but also collaborate with the scientists who seek to use the plant material. Through collaboration, researchers can become aware of and access previously unknown genotypes of interest, while curators expand the use of their collections. While the one-on-one conversation between researcher and curator may be most effective, a majority of collections now have searchable inventories online, making it easy to learn what might be available. Because of their long traditions in horticulture, gardens and other repositories are well equipped to propagate (sexually and asexually) and cultivate fickle genotypes where researchers may have failed. Lastly, all gardens and arboreta (and a growing number of other repositories) have outreach missions which provide collaborating scholars the ability to tap into existing frameworks to facilitate the broader impact requirements associated with grant-funded work. Indeed, maintaining funding and resources for living collections is challenging, and demonstrating research value of collections is one aspect of demonstrating their importance.
While there is no single database encompassing all living collections, the majority of botanical gardens and other repositories maintain online, searchable inventories of their living collections on their institutional webpages. For example, at the Arnold Arboretum, searches can be conducted through a simple query2, as well as through an interactive map known as Collection Researcher3, Repositories within USDA’s NPGS can be searched at http://www.ars-grin.gov/npgs/index.html, and BGCI’s PlantSearch4, has the capability to draw upon over 500,000 records in botanic gardens across the globe. Assuming they already know what they wish to sample, scholars interested in accessing material are best served if they start online to see what taxa are available prior to contacting curatorial staff. Curators can then provide additional documentation as well as work with researchers to further brainstorm about the project, schedule collection dates, and provide other services (see Dosmann, 2006, for examples).
We see great opportunity ahead for genomics-based evo-devo research. Technological advances now provide scientists with a broader array of tools whereby they can rapidly and effectively reach out beyond model organisms, and will find valuable samples that are being grown and/or stored in plant collections. Researchers benefit by not only accessing germplasm of value, but through collaboration with staff who often possess unique expertise complementary to those in the research community. Through these joint efforts, not only can tremendous progress be made in the study of evo-devo, but living collections can successfully expand their utility to wider audiences.
Conflict of Interest Statement
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
We thank Peter Endress, Paul Gepts, Neelima Sinha, and Doug Soltis for sharing experiences and insights concerning the use of living collections in their research. Curatorial work by Michael Dosmann is supported by competitive grants by IMLS, and research by Andrew Groover is supported by competitive grants from USDA NIFA and DOE. This work was inspired by the National Evolutionary Synthesis Center meeting “Evolutionary Origins and Development of Woody Plants,” October 2011.
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