PLANT MOLECULAR EVOLUTION

PLANT MOLECULAR EVOLUTION

Edited by

JEFF J. DOYLE L.H. Bailey Hortorium, Cornell University, Ithaca, New York, USA

and

BRANDON S. GAUT Department of Ecology and Evolutionary Biology, University of California, lrvine, California, USA

Reprinted from Plant Molecular Biology, Volume 42 (1), 2000

SPRINGER SCIENCE+BUSINESS MEDIA, B.V.

Library of Congress Cataloging-in-Publication Data

ISBN 978-94-010-5833-9 ISBN 978-94-011-4221-2 (eBook) DOI 10.1007/978-94-011-4221-2

Printed on acidjree paper

AH Rights Reserved ©2000 Springer Science+Business Media Dordrecht Originally published by Kluwer Academic Publishers in 2000 Softcover reprint of the hardcover 1 st edition 2000

No part of the material protected by this copyright notice may be reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording or by any information storage and retrieval system, without written permission from the copyright owner.

CONTENTS

Preface

Section 1: Molecular evolution and phylogenetics: general issues

Evolution of genes and taxa: a primer

vii-ix

J.J. Doyle, B.S. Gaut 1-23

Examining rates and patterns of nucleotide substitution in plants S.v. Muse 25-43

Contributions of plant molecular systematics to studies of molecular evolution E.D. Soltis, PS. Soltis 45-75

Section 2: Evolution of gene families and gene functions: case histories

Molecular evolution of the chalcone synthase multigene family in the morning glory genome M.L. Durbin, B. McCaig, M.T. Clegg 79-92

Myrosinase: gene family evolution and herbivore defense in Brassicaceae L. Rask, E. Andreasson, B. Ekbom, S. Eriksson, B. Pontoppidan, J. Meijer 93-113

A short history of MADS-box genes in plants G. Theissen, A. Becker, A. Di Rosa, A. Kanno, J.T. Kim, T. MOnster, K.-U. Winter, H. Saedler 115-149

Knots in the family tree: evolutionary relationships and functions of knox homeobox genes L. Reiser, P. Sanchez-Baracaldo, S. Hake

Section 3: The evolution of important phenomena in plants

Evolutionary genetics of self-incompatibility in the Solanaceae A.D. Richman, J.R. Kohn

The evolution of nodulation G. Gualtieri, T. Bisseling

The evolution of disease resistance genes T.E. Richter, PC. Ronald

Hybridization, introgression, and linkage evolution L.H. Rieseberg, S.J.E. Baird, K.A. Gardner

Genome evolution in polyploids J.F. Wendel

Transposable element contributions to plant gene and genome evolution J.L. Bennetzen

Index

151-166

169-179

181-194

195-204

205-224

225-249

251-269

271-272

Cover illustration Ipomoea purpurea Roth, the common Morning Glory. I. purpurea is a bee-pollineated annual vine whose flowers open in the morning and senesce the same day. The purple flower shown is typical of populations of I. purpurea found in Mexico. The species is thought to have spread from a center of origin in central Mexico and is now found as a weed in the southeastern USA. In contrast to Mexican populations there is considerable diversity in flower color in US populations. Durbin et al. examine the evolution and expression of the chalcone synthase multigene family, a key enzyme in flower color biosynthesis. Plant Molecular Biology 42, pp. 79-92.

" Plant Molecular Biology 42: vii-ix, 2000. © 2000 KhlWer Academic Publishers.

Preface

vii

In one sense or another, everything in life is about evolution. Certainly, it is widely accepted that evolution is a primary force that shapes the natural world, starting at the level of individual molecules and building from there to genotypes and the phenotypes they underlie, to populations, species, and still higher taxonomic categories. At the lower end of that spectrum, dynamic in their own right but molded in turn by evolutionary patterns of species, are the complex interrelationships of multigene families. Evolution has always played a part in molecular biology, albeit often in a fairly understated way as in the concept of 'conserved' motifs - TATA boxes and the like. But that role has become increasingly important, as more and more genes from more and more taxa have been described. We are now in the era of comparative genomics, and 'evolutionary' might justifiably be substituted for 'comparative'.

And evolutionary biology is increasingly able to meet the needs of molecular biologists. While development, physiology, and other fields have been transformed by the molecular revolution, evolution and systematics (the study of the kinds and diversity of living things) have experienced their own explosive molecular biology-fueled growth. Molecular technology has given evolutionists the ability, at long last, to look directly at the genotype and cut out the phenotypic middleman; the impact on evolutionary theory has been dramatic. In systematics, the powerful union of such molecular tools as polymerase chain reaction with computer technology has made it possible to look beyond the tips of the 'tree of life' and construct phylogenetic hypotheses for large groups of organisms.

In this issue, we have attempted to give a few examples from among the many interfaces between plant molec­ular biology and evolutionary biology. The field is vast, and we have by no means covered - or even attempted to cover - all of the bases. Some particularly prominent areas are missing entirely, such as the extremely rich area of organellar genome evolution, for which several excellent reviews fortunately exist. The book is organized into three major sections, beginning with some general topics. The editors first present a 'primer' on molecular evolution and systematics, which we hope will be useful to those who may not be fluent with the concepts and terminology of such issues as Neutral Theory, paralogy/orthology, or phylogeny reconstruction. The second paper, by Spencer Muse, contains both a statistical and an empirical component. The statistical component explains some of tools applied to molecular evolutionary inference, while the empirical component summarizes what is known, and unknown, about the pattern and process of nucleotide substitution in plants. The paper discusses such features as variation in rates of evolution among genes and variation in rates of evolution among different plant species. In the final paper of the first section, Doug and Pam Soltis describe the progress being made in molecular phylogenetics of plants. They provide an overview of progress in handling large data sets involving several genes from each of hundreds of species, offering hope that the complexity of such data sets presents not only the obvious advantages of improved sampling and more characters, but even makes possible faster and more thorough analysis. They then update our understanding of the relationships of key plant groups, such as land plants, flowering plants (angiosperms), and, within the angiosperms, families that include important economic or model plants such as maize and Arabidopsis.

The second section presents several case histories describing the evolution of protein-coding gene families - an important topic, because gene families dominate the genomic landscape of plants. In the first paper of this section, Mary Durbin, Bonnie McCaig and Michael Clegg describe their work on the chalcone synthase family in the common morning-glory. A great deal is known about the function of chalcone synthase - it regulates expression of the biochemical pathway that governs flower coloration - but there is still much to learn about the evolution of the gene family. Durbin et al. reveal that the gene family contains highly divergent members, many of which are differentially expressed. The gene family even has 'black sheep', in that some members of the family have

Vlll

been recruited to fill a different functional role. Functional evolution of a gene family is also an important theme of Lars Rask and colleagues, who discuss the biochemistry, molecular evolution, and ecology of the myrosinase family. These genes control the 'mustard oil bomb' pathway characteristic of the Brassicaceae (cabbages, radishes, Arabidopsis, etc.) but which also is found in a small group of related families, including such plants as papaya. The phylogenetic relationships of myrosinases are with the glucosidases involved in the much more widespread and presumably more ancient process of cyanogenesis. This suggests that the cyanogenic pathway was recruited and modified in an ancestor of the mustard oil families, where these active compounds now form the basis of a complex and coevolved network of plant-insect and plant-pathogen interactions.

One of the most studied plant gene families is the MADS-box family, transcription factors best known for their roles in floral development but also active throughout the plant body, even in such tissues as the legume nodule. GUnter Theissen and colleagues provide 'A short history of MADS-box genes in plants' - a voluminous and comprehensive paper, integrating phylogenetic information on MADS genes from ferns, conifers, Gnetales (a group of uncertain placement often thought to be sister to flowering plants), and basal angiosperms to develop hypotheses that link the proliferation of these genes with reproductive innovations culminating in the diversity of modern flowers. Whereas in plants the MADS-box family is probably the best current example of the fusion of evolution, developmental biology, and molecular biology, in animals that distinction is unquestionably held by another family of transcription factors, the homeobox genes, whose role in body plan evolution is the subject of much experimentation and speculation. Plants also have homeobox genes, and the paper by Leonore Reiser, Patricia Sanchez-Baracaldo and Sarah Hake focuses on the Knotted-like (knox) gene family, best known from maize. They discuss expression patterns in the context of repeated duplications of the major classes of knox genes, themselves related by a still more ancient duplication. Phylogenetic trees for the family help identify putatively orthologous genes, while expression studies indicate how homologous copies have evolved over the course of flowering plant evolution, functioning not only in the meristem but in other areas as well.

The third section of the issue makes a transition from single-gene families to address the contributions of molecular and evolutionary approaches to our understanding of several important phenomena in plant biology. The first of these papers, by Adam Richman and Joshua Kohn, deals with self-incompatibility genes in solanaceous species. Instead of focusing on gene function, however, this chapter serves as an example of how genes, and more particularly DNA sequences, can be used to make inferences about species' histories. Richman and Kohn report that the pattern of DNA sequence variation at the self-incompatibility locus varies from species to species. The differences between species can be explained by differences in life history and, as importantly, by historically dif­ferent population sizes. In the second paper of this section, Gustavo Gualtieri and Ton Bisseling treat the evolution of nodulation symbioses in both legumes and non-leguminous plants. They discuss possible structural homologies between rhizobial and actinorhizal nodules, and review evidence suggesting that nodulation could have arisen by recruitment of pre-existing components of the more ancient and taxonomically widespread endomycrorrhizal symbiosis. Symbioses, but of a parasitic rather than mutualistic type, are the focus of the paper in which Todd Richter and Pamela Ronald discuss the evolution of disease resistance genes. These genes usually contain a shared structural motif called the leucine-rich repeat (LRR), but the evolution of the genes varies dramatically according to many factors, including the region of the gene under study, the physical organization of genes (single copy or clustered), and the evolutionary lineage in which they are found. One interesting facet of disease resistance genes is that they appear to evolve so quickly that disease resistance loci are not syntenous over even relatively short evolutionary distances, such as within the grass family.

Linkage relationships across whole genomes are the focus of the next paper, in which Loren Rieseberg, Stuart J.E. Baird, and Keith A. Gardner discuss natural homoploid (i.e. non-polyploid) hybridization, drawing on their extensive studies of genome structure and evolution in both natural and resynthesized Helianthus hybrid species. Among their conclusions are that hybridization can result in major restructuring of the genome and can produce new species rapidly. Many of these same themes are also at the heart of Jonathan Wendel's review of gene and genome evolution in polyploids. The majority - perhaps the vast majority - of flowering-plant genomes have been shaped by polyploid events at some time in their history, making understanding of this process of critical impor­tance. Like hybridization, polyploidy can bring together genes from diverse sources and promote new interactions, but unlike diploid hybrids, polyploids of hybrid origin (allopolyploids) must generally accommodate genes from the homologous (homoeologous) loci of both parents for long periods of evolutionary time. The results for gene

IX

family evolution vary greatly from gene to gene and from species to species, and include new expression patterns, silencing, divergence in function, concerted evolution, and rapid structural changes that may involve transposable element activation and migration. The role of transposable elements in the evolution of genes and genomes is covered in more detail by Jeff Bennetzen in the final paper. Bennetzen catalogs the categories of transposable elements, from DNA transposons to retrotransposons to MITEs. Different elements have different target speci­ficities; for example, MITEs prefer to transpose into genic regions but retrotransposons predominantly insert into other retrotransposons. The overall activity of transposonable elements varies substantially among species but, as Bennetzen details, they are an important component of the structure and evolution of plant genomes.

It is our hope that this overview does not merely provide information about specific topics - though clearly there is plenty of information here. Rather, the goal is to provide examples of studies that cover a range of topics that combine plant molecular biology and evolution. Of the authors, some are primarily molecular biologists, whereas others would no doubt describe themselves as systematists or evolutionary biologists. Thus, in the range of topics and the breadth of the authors' interests we feel that there is something here with which any reader can identify, and, we hope, be stimulated to think about the interface between the different fields.