Plant evolutionary developmental biology

Evolutionary developmental biology (evo-devo) is the study of developmental programs and patterns from an evolutionary perspective. It seeks to understand the various influences shaping the form and nature of life on the planet. Evo-devo arose as a separate branch of science rather recently. An early sign of this occurred in 1999.

Most of the synthesis in evo-devo has been in the field of animal evolution, one reason being the presence of model systems like ''Drosophila melanogaster'', '' C. elegans'', zebrafish and ''Xenopus laevis''. However, since 1980, a wealth of information on plant morphology, coupled with modern molecular techniques has helped shed light on the conserved and unique developmental patterns in the plant kingdom also.

Historical perspective

Before 1900

The origin of the term "morphology" is generally attributed to Johann Wolfgang von Goethe (1749–1832). He was of the opinion that there is an underlying fundamental organisation (') in the diversity of flowering plants. In his book
The Metamorphosis of Plants
', he proposed that the ' enabled us to predict the forms of plants that had not yet been discovered. Goethe was the first to make the perceptive suggestion that flowers consist of modified leaves. He also entertained different complementary interpretations.(for an expanded version of this article see

')

In the middle centuries, several basic foundations of our current understanding of plant morphology were laid down. Nehemiah Grew, Marcello Malpighi, Robert Hooke, Antonie van Leeuwenhoek, Wilhelm von Nageli were just some of the people who helped build knowledge on plant morphology at various levels of organisation. It was the taxonomical classification of Carl Linnaeus in the eighteenth century though, that generated a firm base for the knowledge to stand on and expand. The introduction of the concept of Darwinism in contemporary scientific discourse also had had an effect on the thinking on plant forms and their evolution.

Wilhelm Hofmeister, one of the most brilliant botanists of his times, was the one to diverge away from the idealist way of pursuing botany. Over the course of his life, he brought an interdisciplinary outlook into botanical thinking. He came up with biophysical explanations on phenomena like phototaxis and geotaxis, and also discovered the alternation of generations in the plant life cycle.

1900 to the present

The past century witnessed a rapid progress in the study of plant anatomy. The focus shifted from the population level to more reductionist levels. While the first half of the century saw expansion in developmental knowledge at the tissue and the organ level, in the latter half, especially since the 1990s, there has also been a strong impetus on gaining molecular information.

Edward Charles Jeffrey was one of the early evo-devo researchers of the 20th century. He performed a comparative analyses of the vasculatures of living and fossil gymnosperms and came to the conclusion that the storage parenchyma has been derived from tracheids. His research focussed primarily on plant anatomy in the context of phylogeny. This tradition of evolutionary analyses of plant architectures was further advanced by Katherine Esau, best known for her book ''The Plant Anatomy''. Her work focussed on the origin and development of various tissues in different plants. Working with Vernon Cheadle, she also explained the evolutionary specialization of the phloem tissue with respect to its function.

In 1959 Walter Zimmermann published a revised edition of '. This very comprehensive work, which has not been translated into English, has no equal in the literature. It presents plant evolution as the evolution of plant development (hologeny). In this sense it is plant evolutionary developmental biology (plant evo-devo). According to Zimmermann, diversity in plant evolution occurs though various developmental processes. Three very basic processes are heterochrony (changes in the timing of developmental processes), heterotopy (changes in the relative positioning of processes), and heteromorphy (changes in form processes).

In the meantime, by the beginning of the latter half of the 1900s, ''Arabidopsis thaliana'' had begun to be used in some developmental studies. The first collection of ''Arabidopsis thaliana'' mutants were made around 1945. However it formally became established as a model organism only in 1998.

The recent spurt in information on various plant-related processes has largely been a result of the revolution in molecular biology. Powerful techniques like mutagenesis and complementation were made possible in ''Arabidopsis thaliana'' via generation of T-DNA containing mutant lines, recombinant plasmids, techniques like transposon tagging etc. Availability of complete physical and genetic maps, RNAi vectors, and rapid transformation protocols are some of the technologies that have significantly altered the scope of the field. Recently, there has also been a massive increase in the genome and EST sequences of various non-model species, which, coupled with the bioinformatics tools existing today, generate opportunities in the field of plant evo-devo research.

Gérard Cusset provided a detailed in-depth analysis of the history of plant morphology, including plant development and evolution, from its beginnings to the end of the 20th century. Rolf Sattler discussed fundamental principles of plant morphology and plant evo-devo. Rolf Rutishauser surveyed the past and future of plant evo-devo with regard to continuum and process morphology. The most recent innovation is Articulation Morphology.Articulation Morphology, grounded in the open growth of plants, focuses on ramification as the key principle of plant morphology. This principle entails articulation: the formation of articles. Unlike organs, which are defined in terms of a morphological theory such as the root-stem-leaf model, articles, which have been almost completely overlooked, are directly observable, that is, they are factual and objective. As such, articulation morphology based on articles offers a common foundation for all morphologists, regardless of their theoretical preferences. While so far plant morphology has been centered around homology, articulation morphology shifts the focus to the transformation of ramification and articulation during development and evolution. This shift has far-reaching consequences for plant morphology and plant evo-devo.

Organisms, databases and tools

The most important model systems in plant development have been arabidopsis and maize. Maize has traditionally been the favorite of plant geneticists, while extensive resources in almost every area of plant physiology and development are available for ''Arabidopsis thaliana''. Apart from these, rice, ''Antirrhinum majus'', ''Brassica'', and tomato are also being used in a variety of studies. The genomes of ''Arabidopsis thaliana'' and rice have been completely sequenced, while the others are in process. It must be emphasized here that the information from these "model" organisms form the basis of our developmental knowledge. While ''Brassica'' has been used primarily because of its convenient location in the phylogenetic tree in the mustard family, ''Antirrhinum majus'' is a convenient system for studying leaf architecture. Rice has been traditionally used for studying responses to hormones like abscissic acid and gibberelin as well as responses to stress. However, recently, not just the domesticated rice strain, but also the wild strains have been studied for their underlying genetic architectures.

Some people have objected against extending the results of model organisms to the plant world. One argument is that the effect of gene knockouts in lab conditions wouldn't truly reflect even the same plant's response in the natural world. Also, these supposedly ''crucial'' genes might not be responsible for the evolutionary origin of that character. For these reasons, a comparative study of plant traits has been proposed as the way to go now.

Since the past few years, researchers have indeed begun looking at non-model, "non-conventional" organisms using modern genetic tools. One example of this is the Floral Genome Project, which envisages to study the evolution of the current patterns in the genetic architecture of the flower through comparative genetic analyses, with a focus on EST sequences. Like the FGP, there are several such ongoing projects that aim to find out conserved and diverse patterns in evolution of the plant shape. Expressed sequence tag (EST) sequences of quite a few non-model plants like sugarcane, apple, barley, cycas, coffee, to name a few, are available freely online. The Cycad Genomics Project, for example, aims to understand the differences in structure and function of genes between gymnosperms and angiosperms through sampling in the order Cycadales. In the process, it intends to make available information for the study of evolution of seeds, cones and evolution of life cycle patterns. Presently the most important sequenced genomes from an evo-devo point of view include those of '' A. thaliana'' (a flowering plant), poplar (a woody plant), ''Physcomitrella patens'' (a bryophyte), Maize (extensive genetic information), and '' Chlamydomonas reinhardtii'' (a green alga). The impact of such a vast amount of information on understanding common underlying developmental mechanisms can easily be realised.

Apart from EST and genome sequences, several other tools like PCR, yeast two-hybrid system, microarrays, RNA Interference, SAGE, QTL mapping etc. permit the rapid study of plant developmental patterns. Recently, cross-species hybridization has begun to be employed on microarray chips, to study the conservation and divergence in mRNA expression patterns between closely related species. Techniques for analyzing this kind of data have also progressed over the past decade. We now have better models for molecular evolution, more refined analysis algorithms and better computing power as a result of advances in computer sciences.

Evolution of plant morphology

Overview of plant evolution

Evidence suggests that an algal scum formed on the land , but it was not until the Ordovician period, around , that land plants appeared. These began to diversify in the late Silurian period, around , and the fruits of their diversification are displayed in remarkable detail in an early Devonian fossil assemblage known as the Rhynie chert. This chert preserved early plants in cellular detail, petrified in volcanic springs. By the middle of the Devonian period most of the features recognised in plants today are present, including roots and leaves. By the late Devonian, plants had reached a degree of sophistication that allowed them to form forests of tall trees. Evolutionary innovation continued after the Devonian period. Most plant groups were relatively unscathed by the Permo-Triassic extinction event, although the structures of communities changed. This may have set the scene for the evolution of flowering plants in the Triassic (~), which exploded the Cretaceous and Tertiary. The latest major group of plants to evolve were the grasses, which became important in the mid Tertiary, from around . The grasses, as well as many other groups, evolved new mechanisms of metabolism to survive the low and warm, dry conditions of the tropics over the last . Although animals and plants evolved their bodyplan independently, they both express a developmental constraint during mid-embryogenesis that limits their morphological diversification.

Meristems

The meristem architectures differ between angiosperms, gymnosperms and pteridophytes. The gymnosperm vegetative meristem lacks organization into distinct tunica and corpus layers. They possess large cells called central mother cells. In angiosperms, the outermost layer of cells divides anticlinally to generate the new cells, while in gymnosperms, the plane of division in the meristem differs for different cells. However, the apical cells do contain organelles like large vacuoles and starch grains, like the angiosperm meristematic cells.

Pteridophytes, like fern, on the other hand, do not possess a multicellular apical meristem. They possess a tetrahedral apical cell, which goes on to form the plant body. Any somatic mutation in this cell can lead to hereditary transmission of that mutation. The earliest meristem-like organization is seen in an algal organism from group ''Charales'' that has a single dividing cell at the tip, much like the pteridophytes, yet simpler.
One can thus see a clear pattern in evolution of the meristematic tissue, from pteridophytes to angiosperms: Pteridophytes, with a single meristematic cell; gymnosperms with a multicellular, but less defined organization; and finally, angiosperms, with the highest degree of organization.

Evolution of plant transcriptional regulation

Transcription factors and transcriptional regulatory networks play key roles in plant development and stress responses, as well as their evolution. During plant landing, many novel transcription factor families emerged and are preferentially wired into the networks of multicellular development, reproduction, and organ development, contributing to more complex morphogenesis of land plants.

Evolution of leaves

Origins of the leaf

Leaves are the primary photosynthetic organs of a plant. Based on their structure, they are classified into two types - microphylls, that lack complex venation patterns and megaphylls, that are large and with a complex venation. It has been proposed that these structures arose independently. Megaphylls, according to the telome theory, have evolved from plants that showed a three-dimensional branching architecture, through three transformations: , which involved formation of a planar architecture, webbing, or formation of the outgrowths between the planar branches and fusion, where these webbed outgrowths fused to form a proper leaf lamina.
Studies have revealed that these three steps happened multiple times in the evolution of today's leaves.

Contrary to the telome theory, developmental studies of compound leaves have shown that, unlike simple leaves, compound leaves branch in three dimensions.Rutishauser, R. and Sattler, R. 1997. Expression of shoot processes in leaf development of Polemonium caeruleum. Botanische Jahrbücher für Systematik 119: 563-582. Consequently, they appear partially homologous with shoots as postulated by Agnes Arber in her partial-shoot theory of the leaf. They appear to be part of a continuum between morphological categories, especially those of leaf and shoot. Molecular genetics confirmed these conclusions (see below).

It has been proposed that the before the evolution of leaves, plants had the photosynthetic apparatus on the stems. Today's megaphyll leaves probably became commonplace some 360 , about 40 my after the simple leafless plants had colonized the land in the early Devonian period. This spread has been linked to the fall in the atmospheric carbon dioxide concentrations in the late Paleozoic era associated with a rise in density of stomata on leaf surface. This must have allowed for better transpiration rates and gas exchange. Large leaves with less stomata would have heated up in the sun's rays, but an increased stomatal density allowed for a better-cooled leaf, thus making its spread feasible.

Factors influencing leaf architectures

Various physical and physiological forces like light intensity, humidity, temperature, wind speeds etc. are thought to have influenced evolution of leaf shape and size. It is observed that high trees rarely have large leaves, owing to the obstruction they generate for winds. This obstruction can eventually lead to the tearing of leaves, if they are large. Similarly, trees that grow in temperate or taiga regions have pointed leaves, presumably to prevent nucleation of ice onto the leaf surface and reduce water loss due to transpiration. Herbivory, not only by large mammals, but also small insects has been implicated as a driving force in leaf evolution, an example being plants of the genus ''Aciphylla'', that are commonly found in New Zealand. The now-extinct moas (birds) fed upon these plants, and the spines on the leaves probably discouraged the moas from feeding on them. Other members of ''Aciphylla'' that did not co-exist with the moas were spineless.

Genetic evidences for leaf evolution

At the genetic level, developmental studies have shown that repression of the KNOX genes is required for initiation of the leaf primordium. This is brought about by ''ARP'' genes, which encode transcription factors. Genes of this type have been found in many plants studied till now, and the mechanism i.e. repression of KNOX genes in leaf primordia, seems to be quite conserved. Expression of KNOX genes in leaves produces complex leaves. It is speculated that the ''ARP'' function arose quite early in vascular plant evolution, because members of the primitive group lycophytes also have a functionally similar gene Other players that have a conserved role in defining leaf primordia are the phytohormone auxin, gibberelin and cytokinin.

One feature of a plant is its phyllotaxy. The arrangement of leaves on the plant body is such that the plant can maximally harvest light under the given constraints, and hence, one might expect the trait to be genetically robust. However, it may not be so. In maize, a mutation in only one gene called ''abphyl'' (''abnormal phyllotaxy'') was enough to change the phyllotaxy of the leaves. It implies that sometimes, mutational tweaking of a single locus on the genome is enough to generate diversity. The ''abphyl'' gene was later on shown to encode a cytokinin response regulator protein.

Once the leaf primordial cells are established from the SAM cells, the new axes for leaf growth are defined, one important (and more studied) among them being the abaxial-adaxial (lower-upper surface) axis. The genes involved in defining this, and the other axes seem to be more or less conserved among higher plants. Proteins of the ''HD-ZIPIII'' family have been implicated in defining the adaxial identity. These proteins deviate some cells in the leaf primordium from the default abaxial