Editorial: Genetic Regulatory Mechanisms Underlying Developmental Shifts in Plant Evolution

Full text

EDITORIAL
published: 04 June 2019
doi: 10.3389/fpls.2019.00710
Frontiers in Plant Science | www.frontiersin.org 1June 2019 | Volume 10 | Article 710
Edited by:
Elena M. Kramer,
Harvard University, United States
Reviewed by:
Lachezar A. Nikolov,
University of California, Los Angeles,
United States
Madelaine Elisabeth Bartlett,
University of Massachusetts Amherst,
United States
*Correspondence:
Natalia Pabón-Mora
lucia.pabon@udea.edu.co
Specialty section:
This article was submitted to
Plant Development and EvoDevo,
a section of the journal
Frontiers in Plant Science
Received: 31 March 2019
Accepted: 13 May 2019
Published: 04 June 2019
Citation:
Pabón-Mora N, Di Stilio VS and
Becker A (2019) Editorial: Genetic
Regulatory Mechanisms Underlying
Developmental Shifts in Plant
Evolution. Front. Plant Sci. 10:710.
doi: 10.3389/fpls.2019.00710
Editorial: Genetic Regulatory
Mechanisms Underlying
Developmental Shifts in Plant
Evolution
Natalia Pabón-Mora 1
*, Verónica S. Di Stilio 2and Annette Becker 3
1Instituto de Biología, Universidad de Antioquia, Medellín, Colombia, 2Department of Biology, University of Washington,
Seattle, WA, United States, 3Institute of Botany, Justus-Liebig-Universität Gießen, Giessen, Germany
Keywords: plant development, evo devo, plant evolution, reproductive strategies, developmental modularity
Editorial on the Research Topic
Genetic Regulatory Mechanisms Underlying Developmental Shifts in Plant Evolution
The origin and evolution of land plants was accompanied by major macroevolutionary changes,
including profound shifts in reproductive processes. Originally, plants were heavily dependent on
water for gamete transfer, while later on, male gametes were dispersed by wind or animals within
highly reduced gametophytes. Over time, female gametophyte development was internalized and
sperm motility was lost, requiring a sperm delivery system reaching deep into the maternal tissues
inside a megasporangium that evolved into the ovule in seed plants. Moreover, seed plant embryos
became protected within the seed, which contains a nutritional start-up package for the next
generation. In flowering plants, both gamete- and seed-dispersal mechanisms diversified. A carpel
surrounded the ovules requiring fertilization to occur internally and endosperm developed with the
embryo as a result of double fertilization, presumably reducing the risk of allocating resources to
inviable seeds. Flowers developed unlimited displays for pollination, involving mostly variations in
perianth presentation that include elaborate coloration and symmetry changes. Finally, as carpels
mature into fruits, they showcase a wide array of forms that guarantee optimal seed dispersal.
Elaboration of the vegetative phase of land plants also played a major role in their evolution
and habitat adaptation. For instance, fixed multicellularity in the diploid phase of the life cycle (i.e.,
embryo formation) marks the transition to land. Embryo patterning required the diversification of
cell types, the polarization of stem cell niches in the diploid axis and the occurrence of lateral organs
in response to auxin peaks to form leaf primordia. In the sporophyte, leaves develop from the Shoot
Apical Meristem (SAM) achieving extreme morphological variation. Roots developing from a Root
Apical Meristem (RAM) provided anchoring to the substrate and access to nutrients and water
becoming another key innovation of the independent sporophyte. In parallel, the exposure to new
environments triggered new symbiotic interactions.
Central genes that regulate each of these processes act together in larger gene regulatory
modules and networks, and numerous components and interactions are known in the model plant
Arabidopsis thaliana (thale cress). However, how the gene regulatory modules have arisen over
evolutionary time to enable these evolutionary transitions remains an open question at the core of
plant evolutionary developmental research studies. This special issue collects articles contributing
to this question from different perspectives and systems.

Pabón-Mora et al. Genetic Regulation in Plant Evolution
ORIGINS OF COMPLEXITY: THEORETICAL
APPROACHES AND THE STUDY OF GENE
EVOLUTION OVER DEEP PHYLOGENETIC
TIMESCALES
Complexity in plant body patterning has been addressed from
both morphological and genetic standpoints in this issue. The
article by Benítez et al. aims to understand the mechanisms
responsible for the major body plan transitions in green
algae belonging to different clades and the monophyletic land
plants. They introduce the concept of dynamical patterning
modules (DPMs) which are defined as sets of conserved gene
products and molecular networks, in conjunction with the
physical morphogenetic and patterning processes where they
function. They note that critical DPMs for the evolution of
plants are cell-to-cell adhesion, placement of the cell wall, cell
differentiation, and cell polarity. Analyzing data from broad
phyletic comparisons, they conclude that the same DPM patterns
have emerged many times independently, and that unicellular
plant ancestors already possessed most molecular mechanisms
later co-opted by multicellular plants, regardless of whether the
diploid or haploid life phase is the dominant one. They further
show that plasmodesmata were critical for the evolution of
complex multicellularity in plants.
Yruela et al. highlight the evolution of protein ductility
(intrinsic disorder) in unicellular and multicellular organisms.
Investigating the occurrence of protein ductility associated with
gene duplication led them to conclude that it increases in
concert with organismic complexity. Moreover, the distribution
of intrinsically disordered proteins and residues is not random
but can be correlated with chromosomal rearrangement
during evolution.
Complexity can also be studied in terms of gene regulation
over developmental or evolutionary timescales. Bräutigam and
Cronk examined the role of DNA methylation in gene regulation
to fine-tune developmental plasticity. DNA methylation plays a
role in enlarging the potential of phenotypic expression and the
authors argue for the emergence of the novel research field of
“epi-evo-devo.” Complexity can also be modulated by changes
in developmental timing; Buendia-Monreal and Gillmor set up a
framework in which alterations in the timing of developmental
programs during evolution (also known as heterochrony) led to
changes in the diversification of key innovations such as leaves,
roots, flowers and fruits.
Synapomorphies in plant evolution can also be studied
from the evolutionary perspective of gene lineages controlling
developmental, morphological and physiological changes.
For example, AINTEGUMENTA genes encoding AP2-
type transcription factors play multiple functions in plant
development including the maintenance of stem cell
niches, embryo patterning, lateral organ formation, and
fatty acid metabolism. Dipp-Álvarez and Cruz-Ramírez
provide a comprehensive evolutionary framework for the
ANT gene lineage across streptophytes, where preANT-
like genes are present in the ancestor of embryophytes
and a gene duplication occurs in land plants resulting
in the basalANT and the euANT lineages. Possible
roles facilitated by these transcription factors during the
transition to dry environments include enhanced tolerance
to desiccation, and the establishment and maintenance
of multicellularity.
The above-mentioned articles contribute to a theoretical and
experimental foundation for assessing how major novelties may
have arisen during plant evolution, and how potential fine-tuning
of the genetic components responsible for a trait can lead to
considerable variation in plant body plans.
ORIGIN AND PATTERNING OF THE
GAMETOPHYTE AND SPOROPHYTE IN
EARLY-DIVERGING LAND PLANTS
Three manuscripts focused on early-diverging lineages,
including non-vascular bryophytes and vascular lycophytes.
Flores-Sandoval et al. provide an overview of transcription
factors controlling developmental transitions during the
life cycle of the model liverwort Marchantia polymorpha.
The authors explore differentially expressed genes during
specific developmental time points, resulting in sets of genes
acting exclusively in either gametophyte or sporophyte, in
the reproductive transition or in antheridia or archegonia
development. Their analyses reveals auxin co-expression groups
present in liverworts and mosses that are not dependent on the
single class-C Auxin Response Factor (ARF), which in other
plant groups is directly involved in auxin responses. Moreover,
their data confirm the participation of MpARF3 as a negative
regulator of reproductive transition.
The article by Grosche et al. shows that the common symbiotic
pathway required for the mutualistic interactions between
plants and mycorrhiza and the downstream GRAS-domain
transcription factors important for its establishment were
already present in the land plant ancestor. Using phylogenetic
reconstructions, they showed moss lineage specific gene losses
and expansions as well as absence of symbiotic GRAS TFs
in algae. The ancestral presence of symbiotic GRAS TFs may
have therefore provided a platform for conquering the land by
enhancing microbial interactions. This idea is supported by the
fact that in mosses, gene losses in some lineages coincide with
lack of arbuscular mycorrhiza symbiosis.
A different approach was taken by Augstein and Carlsbecker
who were able to trace roots into two independent origins
in lycophytes and euphyllophytes (which include ferns and
seed plants). They review the anatomical diversity of roots,
emphasizing stele patterning, the auxin pathways in the RAM
in different taxa, the genetic mechanisms involved in stem
cell niche maintenance and the root cap control. Most data
gathered so far comes from Arabidopsis, other Brassicales,
the ferns Azolla filiculoides and Ceratopteris richardii and
the lycophyte Selaginella moellendorfii. However, the authors
emphasize that functional tools for comparative analyses are
needed in lycophytes and ferns in order to establish the
conservatism of such networks across vascular plants.
Frontiers in Plant Science | www.frontiersin.org 2June 2019 | Volume 10 | Article 710

Pabón-Mora et al. Genetic Regulation in Plant Evolution
EVOLUTION OF THE MEGASPORANGIUM
(OVULE) AND MEGAGAMETOPHYTE IN
SEED PLANTS
Gymnosperms showcase unique reproductive features that
include the nourishment of the embryo directly by the female
gametophyte and the nucellus, which play the equivalent role
of the endosperm in angiosperms. Moyano et al. describe
the dismantling of the megagametophyte during germination
of Araucaria angustifolia seeds, focusing on the mechanisms
activating programmed cell death (PCD) and the availability of
proteins, starch and lipid bodies for the developing embryo.
Ovule integuments are another distinctive feature
distinguishing gymnosperms, which have one, from
angiosperms, which have typically two. Integuments protect the
ovules and seeds, define a route for pollen entry and contribute
to seed hydration and dormancy. In an effort to assess the
molecular basis of integument identity Arnault et al. investigate
the expression of integument genes in the early-diverging
angiosperm Amborella trichopoda and conclude that YABBY,
KANADI, and HD-ZIPIII transcription factors have conserved
expression patterns between Amborella and Arabidopsis. Their
data contribute to the reconstruction of molecular mechanisms
for integument identity during the evolution of angiosperms.
Akhter et al. explore the evolution of gene lineages that
exclusively expanded in gymnosperms compared to angiosperms
employing RNA sequencing. They focus on the TM3-like MADS
box genes, from which DAL19 has been previously identified
as being specifically upregulated in cone-setting shoots. They
show the importance of previously unrecognized, and sometimes
mutually exclusive, mRNA splice variants in Picea abies. They
also highlight isoforms that are differentially expressed in male
and female cone meristems, as well as in vegetative meristems.
From their work, we derive that splice variants are in fact another
source of variation contributing to functional evolution, working
in parallel with gene duplication.
EVOLUTION OF MOLECULAR
MECHANISMS UNDERLYING FLOWERING
Gene duplication is a known source for variation and functional
diversification, triggering major evolutionary shifts. Flowering is
one of the most important transitions leading to angiosperms;
during this process, the SAM becomes an inflorescence meristem
that in turn develops floral meristems in its flanks. Lee et al.
exemplify the role of gene duplication in one of the key players
in the transition to flowering, FLOWERING LOCUS C (FLC)
in Boechera stricta (Brassicaceae), resulting in the acquisition of
unique roles in the different paralogs. While one of the paralogs
plays a conserved role delaying flowering, the other has lost its
flowering function altogether. The authors uncover independent
mutations that change the species phenology and provide
evidence for heritable variations in vernalization requirements
and flowering time via FLC in Brassicales.
A mini review by Monniaux and Vandenbussche discusses
perianth evolution. They propose that the perianth is formed
in the outer floral whorls to maintain the stamen and carpel
identity gene’s expression exclusively in the center of the flower.
They evaluate negative regulators of B and/or C-class genes,
especially of the APETALA2 (AP2) type and highlight the need
for a broader comparative framework including early-diverging
angiosperms with and without perianth. Exploring the molecular
mechanism underlying floral organ identity Galimba et al.
investigate the genetic redeployment of B-class genes in apetalous
Thalictrum (Ranunculaceae). Ranunculaceae petals have been
lost repeatedly, presumably in conjunction with the loss of the
petal-specific AP3-III paralog. The authors present evidence for
partial redundancy for stamen identity in the remaining paralogs
and a role for these genes in the ectopic petaloidy of sepals, while
proposing a novel mechanisms of dominant-negative regulation
of B-class genes by a truncated AP3-II ortholog.
Damerval et al. explore the genetic underpinnings of floral
symmetry changes affecting floral display in Proteaceae, an early
diverging eudicot family. They find that in Grevillea juniperina,
adnation of stamens to tepals and asymmetrical growth of the
single carpel contribute to the establishment of floral bilateral
symmetry. An annotated floral transcriptome for G. juniperina
is also presented, with an emphasis on floral MADS-box genes
and TCP Class I and Class II gene expression patterns, the latter
known to control floral bilateral symmetry in core eudicots.
Contributing to a more conceptual understanding of floral
symmetry control, Sengupta and Hileman discuss the idea of
direct transcriptional autoregulation (DTA) of CYCLOIDEA
(CYC) genes. They present in silico predictions and experimental
evidence for DTA in flower symmetry evolution and propose that
CYC autoregulation may have evolved via de novo mutations and
could have played a key role in the origin of monosymmetric
flowers in the Lamiales.
EVOLUTION OF THE GENETIC NETWORK
CONTROLLING FRUIT DEVELOPMENT
A fruit genetic network is well established in Arabidopsis,
but comparative analyses of the key players controlling
histogenesis during fruit development outside Brassicaceae is
still scarce. Zumajo-Cardona et al. present the evolution of the
REPLUMLESS (RPL) gene lineage, focusing on the expression
patterns of RPL homologs in Papaveraceae (a basal eudicot).
Arabidopsis RPL controls the identity of the replum, a medial
persistent fruit layer unique to Brassicaceae fruits. In contrast,
RPL homologs control fruit shedding in rice, whereas in
poppy they are broadly expressed during flower development
and become restricted to the dehiscence zone during fruit
maturation, suggesting shifting roles of RPL genes during
angiosperm diversification.
Maheepala et al. present a characterization of Solanaceae
FRUITFULL (FUL) genes. FUL is responsible for fruit wall
proliferation and for limiting the dehiscence zone in the
Arabidopsis silique. While FUL homologs play the same roles
in dry-fruited Solanaceae, they have taken on new roles
in fleshy fruit development where they regulate aspects of
the ripening processes, such as pigment accumulation. The
Frontiers in Plant Science | www.frontiersin.org 3June 2019 | Volume 10 | Article 710

Pabón-Mora et al. Genetic Regulation in Plant Evolution
authors show that Solanaceae have four FUL paralogs, some
originating as a result of a whole genome multiplication event,
others by tandem duplication and one clade even undergoing
pseudogenization. While some Solanaceae FUL clades appear
to have acquired novel functions in fleshy fruit development,
the molecular mechanisms underlying the FUL function shifts
require additional analyses.
In summary, this research topic explores the genetic
mechanisms controlling key developmental transitions, both
vegetative and reproductive, during plant evolution. It includes
original contributions on a variety of scales and processes: from
factors contributing to multicellularity, to body plan complexity,
developmental plasticity, heterochrony, tolerance to desiccation,
gametophyte to sporophyte transition, establishment of embryo
polarity and elaboration of the apical and root meristems and
symbiotic interactions in early diverging land plants. Recognizing
that reproductive shifts have also occurred in more recent
phylogenetic scales, this collection also includes manuscripts
focusing on the control of flowering, the development of
ovules and perianth, floral symmetry and display and the
elaboration of fruits from carpels aimed at dispersing the next
generation. We hope that such comprehensive overview will be
inspiring and will motivate additional efforts in the scientific
community to continue to explore these processes holistically
across land plants.
AUTHOR CONTRIBUTIONS
NP-M wrote the first draft of this manuscript, VSD and
AB revised it and completed the text. All authors made
direct intellectual contribution to the work and approved it
for publication.
FUNDING
NP-M thanks funding from Universidad de Antioquia
Convocatoria Programáticas 2017-16302 COLCIENCIAS 808
retos de país grant number 111580863819. VSD acknowledges
funding from The Fred C. Gloeckner Foundation, Inc. AB is
grateful for funding from German Research Foundation (DFG),
grant numbers BE2547/12-1,2 and 14-1.
Conflict of Interest Statement: The authors declare that the research was
conducted in the absence of any commercial or financial relationships that could
be construed as a potential conflict of interest.
Copyright © 2019 Pabón-Mora, Di Stilio and Becker. This is an open-access article
distributed under the terms of the Creative Commons Attribution License (CC BY).
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original author(s) and the copyright owner(s) are credited and that the original
publication in this journal is cited, in accordance with accepted academic practice.
No use, distribution or reproduction is permitted which does not comply with these
terms.
Frontiers in Plant Science | www.frontiersin.org 4June 2019 | Volume 10 | Article 710