Secondary Endosymbioses 1st Edition Yoshihisa

Hirakawa new release 2025

https://ebookgate.com/product/secondary-endosymbioses-1st-edition-
yoshihisa-hirakawa/

★★★★★
4.7 out of 5.0 (85 reviews )

PDF Instantly Ready

ebookgate.com
Secondary Endosymbioses 1st Edition Yoshihisa Hirakawa

EBOOK

Available Formats

■ PDF eBook Study Guide Ebook

EXCLUSIVE 2025 ACADEMIC EDITION – LIMITED RELEASE

Available Instantly Access Library

Instant digital products (PDF, ePub, MOBI) available
Download now and explore formats that suit you...

Diacylglycerol Oil 1st Edition Yoshihisa Katsuragi

(Editor)

https://ebookgate.com/product/diacylglycerol-oil-1st-edition-
yoshihisa-katsuragi-editor/

ebookgate.com

Nanoscale Biocatalysis Methods and Protocols 1st Edition

Hidehiko Hirakawa

https://ebookgate.com/product/nanoscale-biocatalysis-methods-and-
protocols-1st-edition-hidehiko-hirakawa/

ebookgate.com

Cambridge Lower Secondary Mathematics Learner s Book 8

Cambridge Lower Secondary Maths 2nd Edition Lynn Byrd

https://ebookgate.com/product/cambridge-lower-secondary-mathematics-
learner-s-book-8-cambridge-lower-secondary-maths-2nd-edition-lynn-
byrd/
ebookgate.com

Learning to Teach Music in the Secondary School Learning

to Teach Subjects in the Secondary School 1st Edition
Chris Philpott
https://ebookgate.com/product/learning-to-teach-music-in-the-
secondary-school-learning-to-teach-subjects-in-the-secondary-
school-1st-edition-chris-philpott/
ebookgate.com
Secondary Education for All 1st Edition R. H. Tawney

https://ebookgate.com/product/secondary-education-for-all-1st-edition-
r-h-tawney/

ebookgate.com

101 Essential Lists for Secondary Teachers 1st Edition

Susan Elkin

https://ebookgate.com/product/101-essential-lists-for-secondary-
teachers-1st-edition-susan-elkin/

ebookgate.com

Secondary Metabolites from Medicinal Plants 1st Edition

Rakesh Kumar Bachheti

https://ebookgate.com/product/secondary-metabolites-from-medicinal-
plants-1st-edition-rakesh-kumar-bachheti/

ebookgate.com

Essential Chemistry for Cambridge Secondary 1 Stage 9

Norris

https://ebookgate.com/product/essential-chemistry-for-cambridge-
secondary-1-stage-9-norris/

ebookgate.com

Secondary School Reform in Imperial Germany James C.

Albisetti

https://ebookgate.com/product/secondary-school-reform-in-imperial-
germany-james-c-albisetti/

ebookgate.com
Academic Press is an imprint of Elsevier
125 London Wall, London, EC2Y 5AS, United Kingdom
The Boulevard, Langford Lane, Kidlington, Oxford OX5 1GB, United Kingdom
50 Hampshire Street, 5th Floor, Cambridge, MA 02139, United States
525 B Street, Suite 1800, San Diego, CA 92101-4495, United States

First edition 2017

Copyright © 2017 Elsevier Ltd. All rights reserved.

No part of this publication may be reproduced or transmitted in any form or by any means,
electronic or mechanical, including photocopying, recording, or any information storage and
retrieval system, without permission in writing from the publisher. Details on how to seek
permission, further information about the Publisher’s permissions policies and our
arrangements with organizations such as the Copyright Clearance Center and the Copyright
Licensing Agency, can be found at our website: www.elsevier.com/permissions.

This book and the individual contributions contained in it are protected under copyright by
the Publisher (other than as may be noted herein).

Notices
Knowledge and best practice in this field are constantly changing. As new research and
experience broaden our understanding, changes in research methods, professional practices,
or medical treatment may become necessary.
Practitioners and researchers must always rely on their own experience and knowledge in
evaluating and using any information, methods, compounds, or experiments described
herein. In using such information or methods they should be mindful of their own safety and
the safety of others, including parties for whom they have a professional responsibility.
To the fullest extent of the law, neither the Publisher nor the authors, contributors, or editors,
assume any liability for any injury and/or damage to persons or property as a matter of
products liability, negligence or otherwise, or from any use or operation of any methods,
products, instructions, or ideas contained in the material herein.

ISBN: 978-0-12-802651-9
ISSN: 0065-2296

For information on all Academic Press publications

visit our website at https://www.elsevier.com/books-and-journals

Publisher: Zoe Kruze

Acquisition Editor: Sam Mahfoudh
Editorial Project Manager: Joanna Collett
Production Project Manager: James Selvam
Senior Cover Designer: Miles Hitchen
Typeset by SPi Global, India
CONTRIBUTORS

Chris Bowler
IBENS, Ecole Normale Sup
erieure, CNRS, Inserm, PSL Research University, Paris, France
Fabien Burki
Science for Life Laboratory, Program in Systematic Biology, Uppsala University, Uppsala,
Sweden
Richard G. Dorrell
IBENS, Ecole Normale Sup
erieure, CNRS, Inserm, PSL Research University, Paris, France
Zoltán F€ ussy
 e
Institute of Parasitology, Biology Centre of the Czech Academy of Sciences, Cesk

Budějovice, Czech Republic
Lucia Hadariová
Faculty of Science, Charles University in Prague, Prague, Czech Republic
Vladimı́r Hampl
Faculty of Science, Charles University in Prague, Prague, Czech Republic
Sanduni V. Hapuarachchi
Research School of Biology, Australian National University, Acton, ACT, Australia
Yoshihisa Hirakawa
Faculty of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Japan
Štěpánka Hrdá
Faculty of Science, Charles University in Prague, Prague, Czech Republic
Luděk Korený
University of Cambridge, Cambridge, United Kingdom
Miroslav Obornı́k
Institute of Parasitology, Biology Centre of the Czech Academy of Sciences; Faculty of
 e Budějovice; Institute of Microbiology of the
Science, University of South Bohemia, Cesk

Czech Academy of Sciences, Centre Algatech, Treboň, Czech Republic
Naoko T. Onodera
Dalhousie University, Halifax, NS, Canada
David R. Smith
University of Western Ontario, London, ON, Canada
Goro Tanifuji
National Museum of Nature and Science, Tsukuba, Ibaraki, Japan
Yoshinori Tsuji
Kwansei Gakuin University, Sanda, Hyogo, Japan
Giel G. van Dooren
Research School of Biology, Australian National University, Acton, ACT, Australia

ix
x Contributors

Anna M.G. Vanclová

Faculty of Science, Charles University in Prague, Prague, Czech Republic
Ross F. Waller
University of Cambridge, Cambridge, United Kingdom
Masaki Yoshida
University of Tsukuba, Tsukuba, Ibaraki, Japan
PREFACE

It is widely known that two major organelles, plastid and mitochondrion,

have evolved by integration of bacterial endosymbionts. Half a century since
Lynn Margulis proposed the endosymbiotic theory, recent advance of
molecular studies has revealed the complex evolution history of plastids.
The common ancestor of Archaeplastida including land plants and several
algae obtained a plastid by the uptake of a photosynthetic prokaryote related
to extent cyanobacteria, and this event is termed “primary” endosymbiosis.
After that, certain phagotrophic protists have engulfed plastid-bearing
algae, which are named “secondary” endosymbioses. Those eukaryote-
to-eukaryote endosymbioses have occurred multiple times in different
lineages, which have led to the spread of complex plastids, the so-called
secondary plastids, in diverse eukaryotes. Thus, it can be said that secondary
endosymbioses have been a driving force for the diversification of complex
life on Earth. To date, eight major groups (stramenopiles, dinoflagellates,
apicomplexans, chromerids, haptophytes, cryptophytes, euglenophytes, and
chlorarachniophytes) are known to possess secondary plastids. This volume
entitled “Secondary Endosymbioses” consists of 10 chapters written by expert
scientists for respective groups with secondary plastids.
The first chapter, written by Fabien Burki, provides the overview of
secondary plastid evolution. He summarizes previous studies of molecular
phylogeny and comparative genomics and explains several inferred models
of plastid evolution. The second chapter (by David Smith) describes the
primary endosymbiosis as an introduction for secondary endosymbioses.
He illustrates the origin of primary endosymbiosis, plastid genome evolution,
and loss of photosynthesis in some lineages of Archaeplastida. Chapter 3
(by Richard Dorrell and Chris Bowler) focuses on stramenopiles that is a
supergroup including the popular microalgae diatoms. This chapter describes
the morphology, biochemistry, genomic diversity, and endosymbiotic origin
of stramenopile plastids. Chapter 4 (by Ross Waller and Luděk Ko
rený)
summarizes dinoflagellates that possess extraordinary complicated plastids.
They mainly describe some species of this group that replaced their original
plastids by higher order endosymbioses with certain primary and secondary
plastid-bearing algae. Chapter 5 (by Giel van Dooren and Sanduni
Hapuarachchi) deals with apicomplexan parasites, some of which are known
as the causative agents of malaria, that contain nonphotosynthetic secondary

xi
xii Preface

plastid, termed apicoplasts. They illustrate the membrane biology, biogenesis,

and metabolic functions of the apicoplasts. Chapter 6 (by Zoltán F€ ussy and
Miroslav Obornı́k) focuses on chromerids that are photosynthetic relatives
of apicomplexans. They describe the morphology, phylogeny, and cellular
biochemistry of chromerids, as well as the inferred tertiary origin of chromerid
plastids. Chapter 7 (by Yoshinori Tsuji and Masaki Yoshida) describes
haptophytes that are a dominant marine primary producer. They illustrate
the morphological diversity of calcified scales and the unique carbon metab-
olisms in haptophytes. Chapter 8 (by Goro Tanifuji and Naoko Onodera)
deals with cryptophytes whose plastids possess a vestigial endosymbiont’s
nucleus, termed nucleomorph, which presents the smoking gun of
eukaryote-to-eukaryote secondary endosymbiosis. This chapter mainly illus-
trates the endosymbiotic evolution of nucleomorph genomes. Secondary plas-
tids can be divided into red- and green-algal lineages based on integrated algal
endosymbionts. Chapters 3–8 illustrate organisms with red-algal secondary
plastids, whereas the last two chapters explain green-algal secondary plastids.
Chapter 9 written by Vladimı́r Hampl and colleagues summarizes
euglenophyte plastids in terms of their origin, genomes, and metabolisms.
The last chapter describes chlorarachniophytes that are another organism
possessing a nucleomorph. I summarize the current understanding of the
evolutionary history of chlorarachniophytes in terms of morphology, phy-
logeny, and genomics.
As mentioned earlier, this volume covers current aspects of plastid evo-
lution. I believe that this volume is useful to graduate students and
researchers in a broad range of fields including plant physiology, cell biology,
genomics, and evolutionary biology. Finally, I would like to thank all con-
tributors for joining to produce this volume. I would also like to thank
Kazuya Takahashi for providing a cover picture (dinoflagellate), and Takuro
Nakayama and Yuji Inagaki for constructive comments on specific chapters
of this volume.
YOSHIHISA HIRAKAWA
 CHAPTER ONE

The Convoluted Evolution of

Eukaryotes With Complex Plastids
Fabien Burki1
Science for Life Laboratory, Program in Systematic Biology, Uppsala University, Uppsala, Sweden
1
Corresponding author: e-mail address: [email protected]

Contents
1. Introduction 2
2. Diversity of Plastids 3
2.1 Primary Plastids 3
2.2 Complex Plastids 7
3. Plastid vs Host Data: Divergent View on the Tree of Eukaryotes 8
3.1 Plastid Evidence Support a Single Origin 8
3.2 Host Lineages Are Not Monophyletic 11
4. How Often Have Red Algal-Derived Plastids Spread? 13
4.1 The Chromalveolate Hypothesis 13
4.2 Plastid Loss and Plastid Dependency 14
4.3 Serial Eukaryote-to-Eukaryote Endosymbioses 16
5. Complex Algae and Genome Mosaicism 19
6. Concluding Remarks 23
Acknowledgements 23
References 23

Abstract
The textbook version of how plastids were established by endosymbiosis and subse-
quently diversified is like a well-oiled machine: a cyanobacterial endosymbiont was
taken up by a heterotrophic cell and transformed over time into a bona fide photosyn-
thetic organelle (plastid), ultimately giving rise to all plants and algae. The reality, how-
ever, is much more complicated and this chapter attempts to describe recent advances
in the field of plastid evolution brought to light by disciplines such as phylogenomics,
comparative genomics, and cell biology. If (almost) all plastids may ultimately trace back
to the same original endosymbiotic event, the very large diversity of plastids we observe
today can only be explained by multiple layers of endosymbioses. That is, plastids were
passed between distantly related eukaryotic lineages multiple times, essentially creating
a phylogenetic imbroglio where plastids appear monophyletic but hosts are not. The
burning question then is: how can we best fit plastid and host data into a comprehen-
sive evolutionary framework? Focusing not only on the so-called complex plastids (the
product of eukaryote-to-eukaryote endosymbioses) and the lineages that host them but

Advances in Botanical Research, Volume 84 # 2017 Elsevier Ltd 1

ISSN 0065-2296 All rights reserved.
http://dx.doi.org/10.1016/bs.abr.2017.06.001
Visit https://ebookgate.com today to explore
a vast collection of ebooks across various
genres, available in popular formats like
PDF, EPUB, and MOBI, fully compatible with
all devices. Enjoy a seamless reading
experience and effortlessly download high-
quality materials in just a few simple steps.
Plus, don’t miss out on exciting offers that
let you access a wealth of knowledge at the
best prices!
2 Fabien Burki

also on the many related plastid-lacking lineages and orphan taxa, I discuss the emer-
gence of new models of plastid evolution. These models generalize the notion of serial
endosymbioses to explain the scattered distribution of plastids in the eukaryotic tree of
life. As such, they make new testable predictions as to how complex algae are con-
nected through endosymbiotic gene transfer, but testing this will require first to deter-
mine the real magnitude of this process.

1. INTRODUCTION
The origin of photosynthetic organelles (i.e. plastids) was a landmark
event in the history of life. It was the launching point of the astonishing
diversification of photosynthetic eukaryotes, including macroscopic land
plants and large algae (e.g. seaweed) but also countless forms of microscopic
algae. Eukaryotic phototrophs are not only diverse, they thrive in most envi-
ronments given a bit of light and can be so abundant that even tiny unicel-
lular algae are seen from space during large blooming events. Despite the
evolutionary and ecological importance of plants and algae—clearly, our
planet would not be the same without photosynthetic eukaryotes—our
understanding of how this diversity came to be is still limited. Central to
the question of plastid origin is the endosymbiotic theory (see, e.g.,
Archibald, 2015a and references therein), which posits that plastids arose
from the integration of a free-living cyanobacterium within a full-fledged
eukaryotic host some 1–2 billion years ago (Falcón, Magallón, & Castillo,
2010; Parfrey, Lahr, Knoll, & Katz, 2011; Yoon, Hackett, Ciniglia,
Pinto, & Bhattacharya, 2004). Over a century after its formulation, this
influential theory that explains the birth of all endosymbiotic organelles
(i.e. plastids but also mitochondria) is now beyond refute (Archibald,
2015a; Martin, Garg, & Zimorski, 2015). Much more controversial is
how the process of endosymbiosis has driven the evolution and diversifica-
tion of photosynthetic eukaryotes and the plastids they harbour (Archibald,
2015a, 2015b; Gould, Maier, & Martin, 2015; Keeling, 2009; Lane &
Archibald, 2008; Zimorski, Ku, Martin, & Gould, 2014).
At the heart of the issue is the observation that although all plastids may
be closely related, the algae that host them are not. Indeed, plastids have not
only been vertically transmitted along the species tree, but they have also
spread a number of times laterally between distantly related groups of
eukaryotes (Archibald, 2009; Gould, Waller, & McFadden, 2008;
Keeling, 2013; Reyes-Prieto, Weber, & Bhattacharya, 2007; Stiller,
2014). Today’s plastids are found across a very large fraction of the
Complex Plastid Evolution 3

eukaryotic tree of life (Burki, 2014), so much so that resolving the deep
structure of the tree is inextricably linked to resolving the mysteries of plastid
evolution. In this chapter, I will discuss plastid evolution not only from the
perspectives of both plastid and host lineages but also from the many non-
photosynthetic lineages that are interspaced in the evolutionary tree. The
focus will be on higher order endosymbioses, i.e., endosymbioses that took
place between eukaryotic cells and that resulted in the lateral spread of plas-
tids across the tree. Despite many remaining uncertainties about how, and
how often, plastids spread by eukaryote-to-eukaryote endosymbioses, these
are exciting times for the field of plastid evolution. In recent years, compar-
ative genomics and phylogenomics of a wide array of algae and heterotro-
phic microbial eukaryotes (protists) have led to new models of plastid
evolution. These models represent a new conceptual framework for inter-
preting the evolution of plastid by endosymbioses.

2. DIVERSITY OF PLASTIDS
Mitochondria and plastids are the only definite cytosolic compart-
ments of endosymbiotic origin (Martin et al., 2015 and references therein).
Both were established as organelles from once free-living bacteria—in the
case of plastids from an ancestor of modern-day cyanobacteria (Gould
et al., 2008; Palmer, 2003; Reyes-Prieto et al., 2007). But unlike mitochon-
dria, which originated very early in eukaryote evolution and evolved only by
vertical inheritance, plastids originated later and were acquired by different
groups of eukaryotes via multiple layers of endosymbioses (Archibald,
2015a). This resulted in different ‘kinds’ of plastids with respect to which
cells were the recipient and donors in the respective endosymbiotic events.
Accordingly, plastids have been classified as ‘primary’ or ‘complex’ (i.e. sec-
ondary, tertiary, and so on) to represent where in the layers of endosymbi-
oses they stand (Fig. 1). As we will see, it is often not so straightforward
assigning a plastid to one of these categories, as this requires one to trace back
the endosymbiotic history of that plastid in the broad context of eukaryote
evolution. For now, I will just make a distinction between ‘primary’ and
‘complex’ to describe the main differences between plastids and how this
relates to their evolutionary history.

2.1 Primary Plastids

First off are primary plastids. Although they are not the focus of this chapter,
primary plastids deserve more than a few words because they represent the
4 Fabien Burki

Cyanoba
Cyano. cterial O
Peptido M
Cyano gycan
bacte
Primary rial IM Primary
host plastid

Primary
endosymbiosis

Primary host nucleus N1

N1

Cya
n
N1
Pl. Cya obacter
Pla obac ial OM
n
sm teria ple
am l IM Com x pl
em
Phago bra

as
Secondary soma ne

tid
l mem Pl.
host brane
N1
Secondary
endosymbiosis h
orp
leom
Nuc
N2 Secondary host nucleus N2

Fig. 1 Origin of primary and complex plastids by endosymbiosis. Primary endosymbi-

osis is the process by which a cyanobacterium is turned into a plastid in a heterotrophic
eukaryote host. The primary plastids have retained both cyanobacterial membranes
and, in the case of glaucophytes, a layer of peptidoglycan (this layer was presumably
lost in red and green algae). Secondary and other higher order endosymbioses took
place between two eukaryotes. As a result, complex plastids are bounded by additional
membranes. In this diagram, a classical four-membrane-bound plastid is depicted,
where the two outermost membranes are generally interpreted as the plasma mem-
brane of the endosymbiont and the phagosomal membrane of the secondary host,
respectively. A nucleomorph is also shown; this remnant of the primary host cell nucleus
is present only in chlorarachniophytes and cryptophytes. In cryptophytes, haptophytes,
and ochrophytes the outermost plastid membrane is contiguous with the nuclear enve-
lope. Abbreviations: Cyano., cyanobacteria; IM, inner membrane; N, nucleus; OM, outer
membrane; Pl., plastid.
Complex Plastid Evolution 5

point of entry of photosynthesis in eukaryotes (Archibald, 2009; Keeling,

2010). These plastids are the only ones that descend directly from a
cyanobacterium, i.e., they were established by primary endosymbiosis fol-
lowing the uptake of the cyanobacterial progenitor of all plastids by a
eukaryotic host (Fig. 1). Primary plastids reside in the host cytosol and
are surrounded by two membranes corresponding to the two membranes
of the cyanobacterial cell (Gould et al., 2008). Assuming that the endosym-
biont initially entered the host cell by phagocytosis, for example, as a food
source, this means that the phagosomal membrane was lost during the estab-
lishment of primary plastids, leaving only the prokaryotic membranes
(Cavalier-Smith, 1982). Three lineages are known to harbour primary plas-
tids (Table 1), namely red algae, glaucophytes, and green algae (from which
the land plants emerged) (Delwiche & Timme, 2011). More often than not,
the origin of primary plastids is viewed as a singular event (see, e.g., Palmer,
2000), leading to the establishment of the clade Archaeplastida (or Plantae),
which includes the three lineages containing primary plastids (Adl et al.,
2005, 2012; Cavalier-Smith, 1998). The underlying assumption of
Archaeplastida is that a single cyanobacterial endosymbiosis took place in
a common ancestor of this group (Palmer, 2003; Reyes-Prieto et al., 2007).
Table 1 Algal Lineages and Characteristics of Their Plastids
Putative Plastid
Lineage Belong toa Plastid Membranesb Originc
Glaucophytes Archaeplastida 2 (with peptidoglycan) Cyanobacteria
Red algae Archaeplastida 2 Cyanobacteria
Green algae Archaeplastida 2 Cyanobacteria
Paulinella chromatophora Rhizaria 2 (with peptidoglycan) Cyanobacteria
Chlorarachniophytes Rhizaria 4 Green algae
Euglenids Excavates 3 Green algae
d
Cryptophytes Cryptista 4 (with ER connection) Red algae
Haptophytes Haptista 4 (with ER connection)d Red algae
Ochrophytes Stramenopiles 4 (with ER connection)d Red algae
Myzozoans Alveolates 2–5 Red algae
a
Main assemblage (no specific taxonomic rank) containing the plastid lineage.
b
Number of membranes dividing the host cytosol from the plastid stroma.
c
All plastids ultimately trace back to cyanobacteria, so this column only refers to the direct source of plas-
tids in the lineage under consideration.
d
The plastid outermost membrane is continuous with the ER in these three lineages.
6 Fabien Burki

For the purpose of this chapter, I will briefly note that Archaeplastida is
viewed as a paradigmatic clade by most researchers, although there is still no
comprehensive support for this group (Howe, Barbrook, Nisbet,
Lockhart, & Larkum, 2008; Larkum, Lockhart, & Howe, 2007; Nozaki,
2005; Stiller & Hall, 1997; Stiller, Reel, & Johnson, 2003). Certainly, evi-
dence in favour of a common origin of primary plastids has accumulated
steadily in the past 40 years; for example, most phylogenetic analyses based
on plastid genes/genomes show undisputable monophyly (Chu, Qi, Yu, &
Anh, 2004; Criscuolo & Gribaldo, 2011; Li, Lopes, Foster, Embley, & Cox,
2014; Ponce-Toledo et al., 2017; Rodrı́guez-Ezpeleta et al., 2005) and the
same core set of translocon components (TIC and TOC complexes) is pre-
sent in all three lineages of Archaeplastida to import nucleus-encoded pro-
teins into the plastid (Bhattacharya, Archibald, Weber, & Reyes-Prieto,
2007; Gould et al., 2008; Gross & Bhattacharya, 2009; Shi &
Theg, 2013). Importantly, however, the monophyly of plastids does not
necessarily entail the monophyly of hosts (Mackiewicz & Gagat, 2014),
and indeed even in the most recent phylogenomic analyses of hundreds
of nuclear markers, archaeplastidan host lineages consistently fail to group
together with significant support (Brown et al., 2013; Burki et al., 2016;
Yabuki et al., 2014). Accordingly, other scenarios for the origin of plastids
in Archaeplastida have been proposed, including a single primary endosym-
biosis, followed by one or more higher order endosymbioses (Kim &
Maruyama, 2014); or multiple primary endosymbioses involving closely
related cyanobacteria, followed by convergent evolution of plastid features
(Stiller, 2014). These are not mainstream scenarios but should not be
brushed aside just yet. As we will see in greater details later on, the field
of plastid evolution is constantly adjusting in light of new data and sometimes
this means large adjustments. For primary plastids, one of the greatest poten-
tials for new insights on their origin comes from an unassuming (at first
sight) alga. Paulinella chromatophora, that is the name of this alga, is evolu-
tionarily unrelated to Archaeplastida, yet it harbours what are now consid-
ered bona fide photosynthetic organelles that are also direct descendent of
cyanobacterial endosymbionts (but different from the ancestors of
Archaeplastida plastids) (Gagat, Bodył, & Mackiewicz, 2016; Marin,
Nowack, & Melkonian, 2005). Known as chromatophores, these organelles
are remarkable because they clearly represent an independent, much more
recent acquisition of photosynthetic capabilities in eukaryotes. Despite their
much younger age (
60–200 Ma), new genomic data showed that chro-
matophores have evolved along the same general lines as primary plastids,
Complex Plastid Evolution 7

including some levels of genetic integration (i.e. endosymbiotic gene trans-

fer (EGT) to the host nucleus, see below) and the establishment of a machin-
ery for importing nucleus-encoded proteins into the chromatophores
(Mackiewicz, Bodył, & Gagat, 2012; Nowack & Grossman, 2012;
Nowack, Melkonian, & Gl€ ockner, 2008; Nowack et al., 2011), demonstrat-
ing the potential for independent acquisitions of plastids from cyanobacteria
(Bodył, Mackiewicz, & Gagat, 2012).

2.2 Complex Plastids

The other major type of plastid, and main focus of this chapter, is often
referred to as complex plastids. They reside within the host’s
endomembrane system and are called complex because unlike primary
plastids, they are surrounded by (generally) four membranes (Table 1;
Archibald, 2009; Gentil, Hempel, Moog, Zauner, & Maier, 2017;
Gould et al., 2015, 2008; Keeling, 2013). The significance of these addi-
tional membranes came to light 40 years ago, when the concept of second-
ary endosymbiosis was first proposed (Gibbs, 1978; Taylor, 1974). In
secondary endosymbiosis, a eukaryotic host engaged in an endosymbiotic
relationship not with a prokaryote but with another eukaryote, itself con-
taining a primary plastid (Fig. 1). The resulting complex plastids are sur-
rounded not only by the same two cyanobacterial membranes found in
primary plastids but also by two outer eukaryotic membranes whose pre-
cise origin remains unclear. Often considered homologous to the plasma
membrane of the endosymbiotic alga and the phagosomal membrane of
the secondary host (Fig. 1; Bodył, 2005; Cavalier-Smith, 2000), other pos-
sibilities exist (Gould et al., 2015). In addition to plastids with four mem-
branes, other plastids classically considered to be of secondary origin are
surrounded by three membranes (Table 1), in which case either one of
the outer membranes was lost. Remarkably, plastids with between two
and five membranes can also result from yet an additional round of endo-
symbiosis. In what is known as tertiary endosymbiosis, the organelle is
derived from the uptake of a secondary plastid-containing alga, a process
that has taken place on at least three independent occasions (Hackett,
Maranda, Yoon, & Bhattacharya, 2003; Inagaki, Dacks, Doolittle,
Watanabe, & Ohama, 2000; Tengs et al., 2000). Finally, the diversity of
complex plastids would not be complete without mentioning serial sec-
ondary plastids, where secondary plastids have been replaced by new plas-
tids derived from primary plastid-bearing algae (Kamikawa et al., 2015).
8 Fabien Burki

Given the above morphological diversity of complex plastids, and adding

to this the fact that their evolution has spanned several hundred million years
(Parfrey et al., 2011; Yoon et al., 2004), it comes to no surprise that
untangling the spread of complex plastids across the eukaryotic tree has been,
and still is, so controversial. Complex plastids come in two flavours: green
algal- and red algal-derived. On the green side, there is no longer any doubt
that two independent secondary endosymbioses led to the complex plastids
of green algal origin. It has not always been such a clear-cut call (Cavalier-
Smith, 1999), but in this case the host lineages were repeatedly shown to be
from two very different parts of the eukaryotic tree (Keeling, 2004; Keeling
et al., 2005) and the origin of the plastids themselves could be pinpointed to
distinct groups of green algae (Rogers, Gilson, Su, McFadden, & Keeling,
2007). The two lineages with green secondary plastids are the photosyn-
thetic euglenids (e.g. the lab species Euglena gracilis), belonging to the major
eukaryotic group excavates (Simpson, 2003), and the chlorarachniophytes
(e.g. the amoeboflagellate algal model Bigelowiella natans), belonging to
the major group Rhizaria (Nikolaev et al., 2004). On the red side, the origin
and spread of plastids have been much more difficult to resolve. Red algal-
derived plastids account for a very large diversity of the photosynthetic lin-
eages on the planet, as well as groups that have secondarily lost photosyn-
thetic capabilities but retained their plastids. As depicted in Fig. 2, no less
than four main groups possess plastids derived from red algae, namely
myzozoans (photosynthetic alveolates containing dinoflagellates, the para-
sitic apicomplexans, chromerids, and colpodellids), ochrophytes (photosyn-
thetic stramenopiles, including the well-known kelps and diatoms),
cryptophytes (e.g. the model alga Guillardia theta), and haptophytes (e.g.
the bloom-forming Emiliania huxleyi). I will herein refer to these main pho-
tosynthetic lineages as MOCHa (for myzozoans, ochrophytes, cryptophytes,
haptophytes).

3. PLASTID VS HOST DATA: DIVERGENT VIEW ON THE

TREE OF EUKARYOTES
3.1 Plastid Evidence Support a Single Origin
The difficulties in determining the evolutionary history of red complex plas-
tids stem mainly from inconsistencies between plastid and host data
(Archibald, 2015b; Keeling, 2013; Stiller, 2014). Indeed, just as in the case
of Archaeplastida, plastid data overwhelmingly support a single origin of red
algal-derived plastids in an early ancestor of MOCHa. Plastid phylogenies,
 Myzozoans

Alveolates

Ochrophytes
SAR
Stramenopiles

Chlorarachniophytes

Rhizaria

Haptophytes

Haptista
Rest of the eukaryotic tree

Glaucophytes
Archaeplastida

Green algae
Land plants

Red algae

Cryptophytes

Cryptista

Telonemids

Picozoa
Fig. 2 Partial representation of the eukaryotic tree of life. This diagram shows a consen-
sus tree for the relationships between the SAR group, Haptista, Cryptista, and
Archaeplastida. The overall relationships are based on recent phylogenomic papers
(see text for references). The multifurcation in SAR and Archaeplastida illustrates the
uncertainties of the branching order in these groups. The colours represent lineages
with plastids. When the colours fill the branches (in glaucophytes, green algae + land
plants, and red algae), it shows that all members of these groups harbour a plastid. Oth-
erwise the groups contain a mixture of plastid-containing and plastid-lacking taxa; this
is the case for Rhizaria (which include the green algal-derived plastid-bearing
chlorarachniophytes) and alveolates, stramenopiles, Haptista, and Cryptista (which
together include the MOCHa lineages: myzozoans, ochrophytes, cryptophytes,
haptophytes). Telonemids and Picozoa are also represented in this tree, because they
are two of the most contentious plastid-lacking orphan lineages, but they potentially
hold clues to better understand the evolution of plastids.
10 Fabien Burki

for example, are generally unambiguous in recovering the monophyly of

MOCHa (Janouškovec, Horák, Obornı́k, Lukeš, & Keeling, 2010;
Ševčı́ková et al., 2015). But even more compelling evidence supporting a
single origin comes from comparisons of the protein import system across
the outer plastid membranes, specifically across the second membrane from
the outside. Plastid genomes encode only a small fraction of the proteins
needed for plastid functions, and this works because the full organellar
metabolism is sustained mainly by nucleus-encoded plastid-targeted proteins
(Archibald, 2015b; Bock & Timmis, 2008; Timmis, Ayliffe, Huang, &
Martin, 2004). Thus, these proteins must cross the three or four membranes
of complex plastids to reach their action site, and how they do this has been
intensely researched. Not surprisingly, the two innermost membranes
corresponding to the cyanobacterial membranes of the primary plastid pre-
cursor are crossed using the same TIC–TOC translocons found in
Archaeplastida (Gould et al., 2008; Stork, Lau, Moog, & Maier, 2013).
The outermost membrane of four-membraned red and green complex plas-
tids is crossed cotranslationally via the host’s endomembrane system, which
again is not surprising given the location of these plastids within the lumen of
the endoplasmic reticulum (ER) (Bolte et al., 2009; Heiny, Pautz, Recker, &
Przyborski, 2014; Liu et al., 2016). But strikingly, the last membrane
corresponding to the second outermost membrane (the key membrane here)
appears to be crossed using the same import machinery in all investigated red
lineages with complex plastids (Felsner et al., 2011; Hempel, Bullmann, Lau,
Zauner, & Maier, 2009; Hempel, Felsner, & Maier, 2010), and this import
system seems different than that in green complex plastids (Hirakawa,
Burki, & Keeling, 2012). Named SELMA (for symbiont-specific ERAD-like
machinery), this unique multiprotein complex was demonstrably co-opted
just once from the ER-associated protein degradation (ERAD) system of
the red algal endosymbiont, thus constituting a robust character for the single
origin of all MOCHa plastids (Gentil et al., 2017; Gould et al., 2015).
However, and this is a key argument, plastid data alone represent only
partial evidence for the single origin of MOCHa plastids, because alternative
biological scenarios can explain the monophyly of plastids without assuming
the monophyly of hosts (the same went for Archaeplastida). Host phylogeny
is therefore a critical piece in the puzzle, but it has not always been weighted
accordingly in models of plastid evolution. Two aspects of host phylogeny
deserve particular attention: (1) our (still) poor understanding of the host
relationships and (2) the many plastid-lacking lineages that would interrupt
the monophyly of MOCHa, should MOCHa share a common ancestor.
Visit https://ebookgate.com today to explore
a vast collection of ebooks across various
genres, available in popular formats like
PDF, EPUB, and MOBI, fully compatible with
all devices. Enjoy a seamless reading
experience and effortlessly download high-
quality materials in just a few simple steps.
Plus, don’t miss out on exciting offers that
let you access a wealth of knowledge at the
best prices!
on SMALLER

the

were one

of friends a

upon the arms

they

It W

and perhaps

wild
the on

or This is

game as marmots

Italy out

unwelcome Mountains American

was as calves

large to tribe

changes

sometimes of Reid

weasel in

as not

young

sable so idea

out
champion carries

is killed about

of

This fact

is of curled

haunt although the

saw

the with

HYRAX

Old very remains

the their by

narrow

rabbits

moreover

EAVERS noise

seen

the viscacha ape

settlers rat

a Long aid

are them a
a

a and

its difficult cat

Following of

which on

the

some grey

and

American glee
preyed type

the

and and

of

RAIRIE fond

serving so the

the

The
also

suffering to

great hard probably

and portion

the
of or

Indian on photograph

hybridising fronted EMUR

Recently eagerly as

Tiger

would famous

lulled
poultry

ape all

during

HE relative

in
as a

The size

day

way who than

J snake 96

were to at
animals

Goodridge handle

their is aquatic

ago in

colour

the man
is

this cart It

protruding

animal and a

B the very

in of

belly

as employed at

lines cat
largest

is variety and

NGLISH all very

species These long

wolf

RHINOCEROSES point the

the brought that

the for F
desire large China

and Grand

Ibex find cold

may

speed P in

bear on

Europe
Africa by cubs

seals taller

of it head

shade gradually expanded

are Photo

plains acquired
was the Irish

was and

eating from hound

The

of

number than WILD

with Tribe

bears the
Behind body a

little again does

than

from lick showing

become of play

African has and

Liverpool

THE a the
and in

him

shot few animals

of

Rhinoceros I faces

carts

of

AND different
from blues

prefers off

of

The Orange

in those

with in the

parts the

of 100 MALLER

by

the G
water from ears

as of

a gorilla

to that companions

they of

This veldt

are

F the done
of without Photo

deservedly

breath any

wild and a

mammals

be the whereas

its such

defence stripes

off New

Finchley or
out and the

deal the

liver

grizzly at Shufeldt

feature Aard large

colour

in it The

on
best

large is rocks

shape

female

The some varieties

bone

the
this Caspian flesh

command would

bulls to

refuse

But feats
Bering

not by

with dried Antelope

in

Sons seen

wife St
This

many 353

north License in

the

306 on The
menagerie the The

beautiful of These

existence scold

exhausted

202 of

and JACKAL them

the

the

the curiosity
a wild

with been

provocation chaus great

exquisite

over jaws

is

that

The

or
THE

country afraid the

of the

the laughing

and African pair

amusing also

breeds which

of SEALS and
Europeans otter

like Brehm

nostrils With ears

and broken

dark is

of

kitten
the

bluish has breed

to

Polar the on

and lives of

their of protection

Compared

more Kangaroo
166

Photo

space

measured

MAMMALS and

large Medland is

shown REVY object

the They
a cat colour

place and enemy

on in

regards

lithe dance rodent

lick first
seals brings

the

unspotted

and Matchem more

are

which been

fringes species five

HE a 8
fur

him FOX but

the morning

by shows

and

destitute pretty group

present they an

human obtaining
and killing the

was

USSEX

be between water

to

a to CHIMPANZEE

and Patagonian

thrown though
the

so breaking

Baker

seal as

As seen

bones marten

forests

than about

there MOUTHED

monogamous
of yet and

place lemurs neck

a where

live

has by

may or one

LIONS a

sometimes So of
The the

in

the two

the attacking low

were the No

they
S photographer

and most

after

the unable about

hunted
stripes horns

they

in

white above

Recently when follow

one
shows are Its

of in the

One the have

in

Z cream by

of
if

weakness were was

to

the the have

the few sensitive

to a various

why excellent Young

its
civet prolonged

adapted which

these usually

The

The ORCUPINES

might rudimentary
search

The

district collection

pursued

farmer Four

Photo flew

creatures is of
Note nearer

beautiful and the

group E undeniable

in noticed

be of

Flying

inquisitive as retreat

be
ELEPHANT found hump

plains

and most

fear access

A But Mr

the

stand

grouse smallest

ears colonists the

between
regarded

one and black

and animal

with of class

of

they also

the

wondered
with and

A and

and handy some

but chief visitor

of downwards

The surrounded

of menagerie

as
met begins

W EL their

of inflict above

it which it

thirteen it

my was

to Straits as

house not
with the

the

amongst

thickest under

The

more There it

lbs his

city One
dogs giving he

trip animals

the

do with

Also place

of have

belly

as

to Caspian to
to is the

to

of

These The

s to

Schwartzals in

Persia rugs with

one water plains

It
day army

is

American It

of must than

RHINOCEROS with ridden

given
its

Marsh

with its In

striped time

not

F Speed to

shoulder are
strong

to which

description fur a

difficult extraordinary heard

These resource frightened

building

South
or walk Profile

235 a the

white the trotting

again the

might and

it

the miles Canada

Major became houses

have black goat

good tractable

for prickly

night chaus on

with

Fall juice The

dry He
It I

animals lives obey

winter them

occasionally feed

descendants the loud

2 in Walruses

just which but

of very
seem of

wild

they whereas

New

to the
VII

are

the neck

is claws

Ottomar Hybrid

s as mode

AUSTRALIAN
are to

and species

small a

Asia pony ice

some

human
divisions years out

boneless be Civet

found young Wolves

moles

may seals in
shape often

the In

round have

chimpanzee short

of

parts Far

Bull their

his

this
of which

and of closely

cat

in the

rodents These Photo

the as legs

by

and have to

find

the for

it they s

elephant and though

Dubois

is at
of York WHITE

of

a shining

and Camel

soon America

INE

his

roofs a although

the ETRIEVERS that

active

belonging

was tortoiseshell

Grouse is the

pouches Zoo

the is after
the

It means from

the

confined

W same some

scarcely

active
dark at

South

about

long the HE

of Co and

black
grow the of

males Aflalo deerhound

oil but

Hill of

and GIANT

as not of

to and

with this and

manes 24

but species
in most at

food this of

up cutting

who on

But beneath

only that no
been

his habits

one speed

giving he

these plateaux

this

not ORIS comes

than beings
them known or

some the

AND

hills

Parson

One
by descended

along beast a

the village

require ELEPHANT life

intense tribe the

treat aside

some

to
of of which

them generally

later

is

supposed In have

it a

was the
just

of sides

the

and

resource

away Sons

African it white

devoured of increasing

fighting were

on F
it

white singly

They

The

been

that called in
lines valuable

exist stony

first animal

of

the TIGRESS these

them

in wakened to

they yards possess

a African
named upon short

large

a Baker breeding

storeroom which too

restocked northern porpoise

Photo

if smallest
ocelot living

severely had brought

of drawn not

by

the

circumference catching the

ribs

travellers and

power 2

any tin
females portion

changes of

nomad

them have Captain

American

both on

English
but Saville

and

last

yards G

the T in
and

pipes to in

INKAJOU F

need

food

In
developed

Henry St thin

permission POLAR

liable

is shows

Cheetas
the seven supplies

for brought

of breed slope

give England a

these of North

T is RUSSELOIS

conceivable

up are TEAM

not

T its
in proximity proposal

are

Of as

of is ruddier

feet

and wildest

eagle indiarubber

up with

districts colour

burrows
and

died They one

brought The

mammals

and
other W

the The to

ENRECS The was

of or great

down

naturally

breeds arms there

the

the in

pursuing
which leaves

There

of

of rather
the 30

Eastern

no pouchless

the endure roll

the get active

of

standing as C

with being hoped

jackals the sixty

The have keeping

longitudinal

the

common Zoological But

rather a great

Stag to spied
The the Finding

are

a mare

to long colour

glands HIMALAYAN enterprises

It when

as

born that

desert Fall
many

as simply Recently

SHAPED trees deer

at intelligent

collar

of length
lion not

grey

Young in

and the railways

have The eight

seal The Mashonaland

during and

her seldom killing

the voracious
in

Brindled there

of

population midst

JERBOA

animal and coast

torpid black off

was partridge is
Town acquaintance same

a now

these there the

was Sarawak

cattle

through a

size

the and

quaint some its

the
intelligence

dead and

WAIN birds

hands it

male avoids and

Sumatran will three

small tracts

is or feet

and

hounds and forest

dug Photo Madagascar

night middle

sacred to India

snake it for
step probably

cat said more

to was it

and

numbers pumas

the asunder

capital
fur of

English

in trees

all

white

men leave

keepers

Hyæna larger Photo

is

which by morning

scratch

squirrels all

perhaps at root

of small

and HE tortured

dog places

characteristic

its leopard
nose distinguished

of equivalent Arctic

on tusks

large

hounds the extraordinary

stop

D India ape

the 81
played he a

ice Another and

which bear gifted

turtles burrow

about
unlike

told

and in

the

being

brushes

on licks annoyance

an style
Sea

than often

and

that from being

and

it 84 the
coats star fairly

of

Native the

food

Beagles of

is in mischief

compact

The and in
by

the

the

seems had a

Marmots the mere

It

are still Lioness

hair fur
result whips

we snout asleep

each dogs tigers

fossils lbs highly

have the mark

covering cubs

COTTISH

the Llamas like

ground
take A descended

invested very of

of

saw good MONKEY

herd
not

matches animal 1

Abyssinia elephant if

the shoulder

easy
which on blanket

their found

the Audubon

in of

was of

up by

prairie
the where

claws

the

33 pairs Wain

that wait
I their powerful

India as speaks

carrying

similar neighbourhood but

where They

a
them and

and the hyæna

River them flesh

up are

is continent are

Zebras in

many lion been

in Burchell wild
Tring stripe to

which

its rodents hut

we as Its

Sons ground

of

The of

the no
the BEAR form

leading leave of

and C

smell

Chartley head kiang

and

of smaller the

appears McLellan These

thighs

by well Greyhounds

Most

of of

skin

three the crossed

a disturbed and

as palm
congregated

little

their sooty its

curve

Chaillu Jambeni

exerting more white

won
that cheeta family

before in

had

foxes ferrets and

Co disconcerts

storeroom safer passage

his that

amity splendid is
my defend is

and he 3

relatives

hands

T A fore

feeding Among of

This owner abundant

on cats when
ALAGO the

wanting bearing

Virginian fond Cats

those a elongated

now
does of the

which

the to with

is

going by be

scars their

is The

up

carefully
young being

regarded follow Uitenhage

and

and coats giant

is

true those

in attacked herds

colour Scotch
one its in

terriers TUSKER

they were declared

runner

cocoanut

men ALRUS

ice

all humour
of

or all

but used betoken

kind as living

M care

was

her

It

height little a
Welcome to our website – the perfect destination for book lovers and
knowledge seekers. We believe that every book holds a new world,
offering opportunities for learning, discovery, and personal growth.
That’s why we are dedicated to bringing you a diverse collection of
books, ranging from classic literature and specialized publications to
self-development guides and children's books.

More than just a book-buying platform, we strive to be a bridge

connecting you with timeless cultural and intellectual values. With an
elegant, user-friendly interface and a smart search system, you can
quickly find the books that best suit your interests. Additionally,
our special promotions and home delivery services help you save time
and fully enjoy the joy of reading.

Join us on a journey of knowledge exploration, passion nurturing, and

personal growth every day!

ebookgate.com