Plant evolutionary developmental biology

Source: Wikipedia, the free encyclopedia.
For a more ecological discussion on the evolution of plant morphology, see Evolutionary history of plants.

Evo-devo arose as a separate branch of science rather recently. An early sign of this occurred in 1999.[2]

Most of the synthesis in evo-devo has been in the field of

plant kingdom also.[3][4]

Historical perspective

Before 1900

Johann Wolfgang von Goethe first used the word morphology.

The origin of the term "

leaves. He also entertained different complementary interpretations.[6][7]

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.[8] 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.

geotaxis, and also discovered the alternation of generations in the plant life cycle.[5]

1900 to the present

Arabidopsis thaliana, a flowering plant that has been a model system for most of plant molecular studies

The past century witnessed a rapid progress in the study of

organ
level, in the latter half, especially since the 1990s, there has also been a strong impetus on gaining molecular information.

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,[11] she also explained the evolutionary specialization of the phloem
tissue with respect to its function.

In 1959 Walter Zimmermann published a revised edition of Die Phylogenie der Planzen.[12] 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).[13]

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.[14] However it formally became established as a model organism only in 1998.[15]

Wikispecies has information related to Arabidopsis thaliana.

The recent spurt in information on various plant-related processes has largely been a result of the revolution in

RNAi vectors, and rapid transformation protocols are some of the technologies that have significantly altered the scope of the field.[15] Recently, there has also been a massive increase in the genome and EST sequences[17] 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.[18] Rolf Sattler discussed fundamental principles of plant morphology[19][20] and plant evo-devo.[21][22][23] Rolf Rutishauser surveyed the past and future of plant evo-devo with regard to continuum and process morphology.[24]

Organisms, databases and tools

The sampling of the Floral Genome Project

The most important

domesticated rice strain, but also the wild strains have been studied for their underlying genetic architectures.[26]

Some people have objected against extending the results of

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.[27]

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

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

computer sciences
.

Evolution of plant morphology

Overview of plant evolution

Main article: Evolutionary history of plants

Evidence suggests that an algal scum formed on the land 1,200 million years ago, but it was not until the Ordovician period, around 500 million years ago, that land plants appeared. These began to diversify in the late Silurian period, around 420 million years ago, and the fruits of their diversification are displayed in remarkable detail in an early

embryogenesis that limits their morphological diversification.[32][33][34][35][36]

Meristems

The

vacuoles and starch
grains, like the angiosperm meristematic cells.

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
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.[38]

Evolution of leaves

For the evolution of photosynthesis, see Photosynthesis.

Origins of the leaf

Further information:
Microphyll
Leaf lamina. The leaf architecture probably arose multiple times in the plant lineage

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.[40]

Contrary to the telome theory, developmental studies of compound leaves have shown that, unlike simple leaves, compound leaves branch in three dimensions.[41][42] Consequently, they appear partially homologous with shoots as postulated by Agnes Arber in her partial-shoot theory of the leaf.[43] They appear to be part of a continuum between morphological categories, especially those of leaf and shoot.[44][45] Molecular genetics confirmed these conclusions (see below).

It has been proposed that the before the evolution 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.[46][47]

Factors influencing leaf architectures

Various physical and physiological forces like

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.[48]

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

gibberelin and cytokinin
.

The diversity of leaves

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.[50]

Once the leaf primordial cells are established from the SAM cells, the new

stomata all over, and not optimized as much for light harvesting
.

How the infinite variety of plant leaves is generated is a subject of intense research. Some common themes have emerged. One of the most significant is the involvement of KNOX genes in generating

EST
sequences involved in the process coming online.

Molecular genetics has also shed light on the relation between radial symmetry (characteristic of stems) and dorsiventral symmetry (typical for leaves). James (2009) stated that "it is now widely accepted that... radiality [characteristic of most shoots] and dorsiventrality [characteristic of leaves] are but extremes of a continuous spectrum. In fact, it is simply the timing of the KNOX gene expression!"[54] In fact there is evidence for this continuum already at the beginning of land plant evolution.[55] Furthermore, studies in molecular genetics confirmed that compound leaves are intermediate between simple leaves and shoots, that is, they are partially homologous with simple leaves and shoots, since "it is now generally accepted that compound leaves express both leaf and shoot properties”.[56] This conclusion was reached by several authors on purely morphological grounds.[41][42]

Evolution of flowers

For a more ecological discussion on the evolution of flowers, see
Evolution of plants § Evolution of flowers
.
The pollen-bearing organs of the early flower Crossotheca

Flower-like structures first appear in the fossil records some ~130 mya, in the Cretaceous era.[57]

The flowering plants have long been assumed to have evolved from within the

gymnosperms to ~300 mya[61]

Traditional view

Cycads

Ginkgo

Conifers

Anthophytes

Bennettitales

Gnetales

Angiosperms

Modern view

Angiosperms

Gymnosperms

Cycads

Bennettitales

Ginkgo

Conifers

Gnetales

Phylogeny of anthophytes and gymnosperms based on Crepet et al. (2000)[62]

The main function of a flower is

angiosperms, was the job of microsporophylls and megasporophylls. A flower can be considered a powerful evolutionary innovation
, because its presence allowed the plant world to access new means and mechanisms for reproduction.

Origins of the flower

It seems that on the level of the organ, the

gymnosperms. Expression of Arabidopsis thaliana LFY in distant plants like poplar and citrus also results in flower-production in these plants. The LFY gene regulates the expression of some gene belonging to the MADS-box
family. These genes, in turn, act as direct controllers of flower development.

Evolution of the MADS-box family

The members of the

transcription factors, that are members of the MADS-box family. Among these, the functions of the B and C domain genes have been evolutionarily more conserved than the A domain gene. Many of these genes have arisen through gene duplications
of ancestral members of this family. Quite a few of them show redundant functions.

The evolution of the

stamens, the male reproductive organ. Thus, the same, then-existing components were used by the plants in a novel manner to generate the first flower. This is a recurring pattern in evolution
.

Factors influencing floral diversity

The various shapes and colors of flowers

How is the enormous diversity in the shape, color and sizes of flowers established? There is enormous variation in the developmental program in different plants. For example,

dicot petals and carpels respectively. It turns out that this is true, and the variation is due to slight changes in the MADS-box genes and their expression pattern in the monocots. Another example is that of the toad-flax, Linaria vulgaris, which has two kinds of flower symmetries: radial and bilateral. These symmetries are due to changes in copy number, timing, and location of expression in CYCLOIDEA, which is related to TCP1 in Arabidopsis.[57][65]

petals in roses
has probably been a result of human selection.

Arabidopsis thaliana has a gene called

genes controlling their development.[67]

Some of these changes also cause changes in expression patterns of the developmental genes, resulting in different

monocots, and also in some basal angiosperms like Amborella. Different models of flower development like the fading boundaries model, or the overlapping-boundaries model which propose non-rigid domains of expression, may explain these architectures.[68]
There is a possibility that from the basal to the modern angiosperms, the domains of floral architecture have gotten more and more fixed through evolution.

Flowering time

Another floral feature that has been a subject of

tropical varieties and common lab strains, do not. Much of this variation is due to mutations in the FLC and FRIGIDA genes, rendering them non-functional.[69]

Many genes in the flowering time pathway are conserved across all plants studied to date. However, this does not mean that the mechanism of action is similarly conserved. For example, the monocot rice accelerates its flowering in short-day conditions, while Arabidopsis thaliana, a eudicot, responds to long-day conditions. In both plants, the proteins CO and FT are present but in Arabidopsis thaliana CO enhances FT production, while in rice the CO homolog represses FT production, resulting in completely opposite downstream effects.[70]

Theories of flower evolution

Main article: Evolutionary history of plants § flowers

There are many theories that propose how flowers evolved. Some of them are described below.

The

megasporangium is covered by three envelopes, like the ovary structure of angiosperm flowers. However, many other lines of evidence show that gnetophytes are not related to angiosperms.[62]

The Mostly Male Theory has a more genetic basis. Proponents of this theory point out that the gymnosperms have two very similar copies of the gene LFY while angiosperms only have one.

pollinators
, but sometime later, may have been integrated into the core flower.

Evolution of secondary metabolism

neem
plant, which helps ward off microbes and insects. Many secondary metabolites have complex structures.

Plant

Cyanogenic glycosides may have been proposed to have evolved multiple times in different plant lineages, and there are several other instances of convergent evolution. For example, the enzymes for synthesis of limonene – a terpene – are more similar between angiosperms and gymnosperms than to their own terpene synthesis enzymes. This suggests independent evolution of the limonene biosynthetic pathway in these two lineages.[73]

Mechanisms and players in evolution

secondary structure of a pri-microRNA from Brassica oleracea

While environmental factors are significantly responsible for evolutionary change, they act merely as agents for

epigenetic
changes. While the general types of mutations hold true across the living world, in plants, some other mechanisms have been implicated as highly significant.

polypoidy
.

teosinte; right: maize
; middle: maize-teosinte hybrid

In recent times, plants have been shown to possess significant microRNA families, which are conserved across many plant lineages. In comparison to animals, while the number of plant miRNA families is less, the size of each family is much larger. The miRNA genes are also much more spread out in the genome than those in animals, where they are found clustered. It has been proposed that these miRNA families have expanded by duplications of chromosomal regions.[74] Many miRNA genes involved in regulation of plant development have been found to be quite conserved between plants studied.

teosinte. Teosinte belongs to the genus Zea, just as maize, but bears very small inflorescence
, 5–10 hard cobs, and a highly branched and spread-out stem.

Cauliflower – Brassica oleracea var. botrytis

Crosses between a particular teosinte variety and maize yield fertile offspring that are intermediate in

QTL analysis has also revealed some loci that when mutated in maize yield a teosinte-like stem or teosinte-like cobs. Molecular clock analysis of these genes estimates their origins to some 9000 years ago, well in accordance with other records of maize domestication. It is believed that a small group of farmers must have selected some maize-like natural mutant of teosinte some 9000 years ago in Mexico, and subjected it to continuous selection to yield the maize plant as known today.[75]

Another case is that of cauliflower. The edible cauliflower is a domesticated version of the wild plant Brassica oleracea, which does not possess the dense undifferentiated inflorescence, called the curd, that cauliflower possesses.

Wikispecies has information related to Brassicaceae.

Cauliflower possesses a single mutation in a gene called CAL, controlling meristem differentiation into inflorescence. This causes the cells at the floral meristem to gain an undifferentiated identity, and instead of growing into a flower, they grow into a lump of undifferentiated cells.[76] This mutation has been selected through domestication at least since the Greek empire.

See also

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Further reading
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