News

Using genomics to learn more about the elusive marsupial mole

A bizarre animal even for Australian standards, the aptly named marsupial mole looks like a mole, but is in fact a marsupial.
Very little is known about this animal in part because only five to ten specimen are seen per decade. With its new genome Dr. Liliya Doronina performed a retrophylogenomic analysis to confirm that Peramelemorphia (bandicoots and bilbies) is the closest sister clade to the marsupial mole. She further went on to use MSMC analyses to study the changing population dynamics of its historic population size during the late Pleistocene and early Holocene. In collaboration, Dr. Sarah Lucas studied the changes within the eye genes of the marsupial mole and revealed a potential trend in which the parts of the eye were released from constraint, starting with the lens, then the cones, and finally the rods.

Read the paper here!
 

The DFG priority program "Genomic Basis of Evolutionary Innovations (GEvol)" SPP (SPP 2349) started in September 2022 with a kick-off meeting in the castle in Münster, had the first annual meeting in the Museum Alexander König in Bonn, and came together again in Frankfurt for the second annual meeting. Over three days, the more than 40 members of the 17 different funded projects presented the current progress of their projects, got involved in lively conversations over lunch or dinner, and talked about further possible collaborations. It was a special pleasure to welcome Dr Breitkreuz from the DFG and our guests Prof Ulrich Krohs from the University of Münster with a talk on "Function and Innovation", Prof Kristen Panfilio (University of Hohenheim) talking about Good Practices for Comparative Insect Genomics, and Prof Clement Gilbert ("Horizontal transfer of transposable elements") from the Université Paris-Saclay. Prof Eyal Privman (University of Haifa) gave another interesting talk on "Social Chromosomes: Variations and Evolution" and Dr Nikolai Hecker from KU Leuven rounded off the 2024 GEvol meeting with a technical talk on "Deep learning, single-cell, and spatial omics to compare cell types across species".

How antisense transcripts can evolve to encode novel proteins.

Bharat Ravi , Anna Grandchamp , Erich Bornberg-Bauer (2024)
https://doi.org/10.1038/s41467-024-50550-3

New protein coding genes can emerge de novo, overlapping existing protein genes but in the opposite (antisense) orientation. The authors Bharat Ravi and Anna Grandchamp from the Bornberglab investigated the possibility of such events using mathematical modelling and data analysis, and found that emergence of a protein coding region (ORF) is generally more likely in one frame of overlap (frame 1), than in the other two frames of overlap and in non-overlapping intergenic regions.

1. The DFG priority program "Genomic Basis of Evolutionary Innovations (GEvol)" SPP (SPP 2349) invites proposals for the second three year funding period starting in late 2025. 

Click here to get more information!

2. Call for papers on the "Genomic Basis of Evolutionary Innovations within Insects" within the Journal of Experimental Zoology-B.

JEZ-B: Molecular and Developmental Evolution is calling for submissions of original studies that describe new experimental and computational techniques, which provide exciting opportunities to study the evolutionary history of genomes using comparative genomics. These new tools help to reconstruct the emergence of new traits from an integrated, phylogenomic perspective, far beyond the limited perspective of individual model species.

New methods (e.g. genomics, transcriptomics and epigenomics)in the insect taxon of interest will reveal the genomic innovations underlying trait evolution, including the roles of: coding vs. regulatory changes, transposable elements, epigenetic regulation, gene family evolution, copy number dynamics, and structural genomic rearrangements. Comparative approaches will reveal the genomic dynamics, which underlie the evolution of novel traits. Such traits may include but are not limited to gain and loss of sociality or mating systems; evolution of complex systems of communication, interaction, defense and immunity; developmental and morphological innovations or phenotypic plasticity.

Submission Deadline: Thursday, 31 October 2024
Click here for more Information!

Complete Sex Chromosomes of Great Apes sequenced... and they are de novo genes!

This year, the complete X and Y chromosomes from living great apes were sequenced and published, lead by the Makova Lab. The Bornberglab is very happy to have contributed a small analysis on de novo genes in this huge and important study. Dr. Margaux Aubel from the Bornberglab was able to detect de novo genes on the highly repetitive and fast evolving Y chromosomes of some of the great apes. One of the de novo genes (shown in the figure) had been duplicated many times in bonobo, similar to the highly duplicated Y chromosome-specific genes called ampliconic genes.

https://www.nature.com/articles/s41586-024-07473-2

New paper out in Nature Communications on the invasion of SARS-CoV-2 variants (https://www.nature.com/articles/s41467-024-46345-1). The study examines the factors contributing to the silent circulation of the Alpha variant before its identification. Depending on the country, the variant has been estimated to circulate up to 60 days before detection. Parts of the study are based on a previous model developed by Pete Czuppon and coauthors (https://royalsocietypublishing.org/doi/full/10.1098/rsif.2021.0575), which has also been recently applied to the question of the first SARS-CoV-2 case (https://journals.plos.org/ploscompbiol/article?id=10.1371/journal.pcbi.1011934).

Leaking marine dumped munition in the North and Baltic Sea and potential effects on fish

Jörn Peter Scharsack, Thünen Institute of Fisheries Ecology, Bremerhaven

Huge amounts of munition ended up on the sea floors, due to military activity and dumping of unused munitions after the world wars. Current estimates encompass about 1.6 mio tonnes munition in German areas of the North and Baltic Sea. As a consequence of ongoing corrosion of munition shells, toxic substances such as the explosive TNT (trinitrotoluene) are leaking into the environment and can be detected in water samples and in biota. This raises concerns about possible negative effects on the environment and inhabiting biota including fish, and last but not least, seafood consumers. This presentation gives an overview about the current state of research on marine dumped munition with special emphasis on fish.
https://conmar-munition.eu/de/
 

Together with the KHlab in Prague we published our study on de novo proteins compared to random proteins. De novo gene emergence provides a route for new proteins to be formed from previously non-coding DNA. Proteins born in this way are considered random sequences and typically assumed to lack defined structure. Taking putative de novo proteins identified in human and fly, we experimentally characterize a library of these sequences to assess their solubility and structure propensity. We compare this library to a set of synthetic random proteins with no evolutionary history. Bioinformatic prediction suggests that de novo proteins may have remarkably similar distributions of biophysical properties to unevolved random sequences of a given length and amino acid composition. However, upon expression in vitro, de novo proteins exhibit moderately higher solubility which is further induced by the DnaK chaperone system. We suggest that while synthetic random sequences are a useful proxy for de novo proteins in terms of structure propensity, de novo proteins may be better integrated in the cellular system than random expectation, given their higher solubility.

Further Information

• Bornberglab
• Original publication

Prof. Dr. Kai Müller, Director of the Botanic Garden at Münster University, is the new President of the Association of Botanic Gardens (VBG). This means that Münster now plays a central role in the network of botanic gardens. Practically all botanic gardens in the German-speaking world are organised in the VBG without exception, but also some gardens from more distant countries. Currently, more than 100 institutions are members of the association, with thousands of employees (gardeners, technical directors, curators, scientific staff, etc.) who can take advantage of the offers of the association or actively participate in the numerous working groups of the association; in addition, there are more than 400 personal memberships and other supporters.  
The VBG represents the interests of its members both nationally and internationally. It is committed to the conservation of biological diversity and is guided by the 17 Sustainable Development Goals of the United Nations and the National Strategy for Biological Diversity. For representatives from politics and business, from authorities at federal, state and district level or other interest groups, the VBG represents an open and competent contact for joint projects or other concerns of botanic gardens.

The new priority program "Genomic Basis of Evolutionary Innovations (GEvol)" SPP (SPP 2349) sponsored by DFG started in September 2022 with a kick-off meeting in the castle in Münster. Over three days, the more than 40 members of the 17 different funded projects had time to introduce their projects, get to know each other over finger food and wine, and talk about their planned research and possible collaborations. It was a special pleasure to welcome Dr Breitkreuz from the DFG and our guests Prof. Klaus Reinhold from Bielefeld University and Dr Julien Dutheil from the MPI in Plön.
 

The DFG-funded CRC/Transregio SFB/TRR 212 (NC3) is being prolonged

The CRC/Transregio "A Novel Synthesis of Individualisation across Behaviour, Ecology and Evolution: Niche Choice, Niche Conformance, Niche Construction (NC³)" has been running since 2018 and has now been prolonged until 2025. It is a research alliance between the Universities of Bielefeld and Münster in the fields of Behavior, Ecology and Evolution. The aim of NC3 is to define and establish the concept of ‘niche’ at the level of the individual organism. NC³ is led by Prof. Oliver Krüger (Bielefeld) as the spokesperson and Prof. Joachim Kurtz (Münster, IEB) as the vice spokesperson. Five of the 20 research project funded within NC³ are in the IEB, and address niche choice, niche conformance and niche construction in diverse organisms. A number of PhD and postdoc position are now available within these projects.

Press release of the WWU: https://www.uni-muenster.de/news/view.php?cmdid=12203

Job offers:
PhD position 65%;
2nd PhD position 65%;
PostDoc position 100%
2nd PostDoc position 100%
 

Inquiline ants are highly specialized and obligate social parasites that infiltrate and exploit colonies of closely related species. They have evolved many times convergently, are often evolutionarily young lineages, and are almost invariably rare. Focusing on the leaf-cutting ant genus Acromyrmex, we compared genomes of three inquiline social parasites with their free-living, closely-related hosts. The social parasite genomes show distinct signatures of erosion compared to the host lineages, as a consequence of relaxed selective constraints on traits associated with cooperative ant colony life and of inquilines having very small effective population sizes. We find parallel gene losses, particularly in olfactory receptors, consistent with inquiline species having highly reduced social behavioral repertoires. Many of the genomic changes that we uncover resemble those observed in the genomes of obligate non-social parasites and intracellular endosymbionts that branched off into highly specialized, host-dependent niches.

For the full paper, please click here.

Online article on WWU news page

 

Comparative genomic studies have repeatedly shown that new protein-coding genes can emerge de novo from noncoding DNA. Still unknown is how and when the structures of encoded de novo proteins emerge and evolve. Combining biochemical, genetic and evolutionary analyses, we elucidate the function and structure of goddard, a gene which appears to have evolved de novo at least 50 million years ago within the Drosophila genus. Previous studies found that goddard is required for male fertility. Here, we show that Goddard protein localizes to elongating sperm axonemes and that in its absence, elongated spermatids fail to undergo individualization. Combining modelling, NMR and circular dichroism (CD) data, we show that Goddard protein contains a large central α-helix, but is otherwise partially disordered. We find similar results for Goddard’s orthologs from divergent fly species and their reconstructed ancestral sequences. Accordingly, Goddard’s structure appears to have been maintained with only minor changes over millions of years.

For the full paper, please click here.


 

How genomes evolve and drive novelty is a central question in biology.
Some of the most puzzling genomic innovations, for example the development of placenta in mammals, are triggered by Transposable Elements (TEs). TEs are small genome fragments that can move and insert in other areas of the genome, which can create or impair gene functions. Organisms have adapted mechanisms to counteract the harmful effects of TEs, notably small RNAs (e.g. piwi-interacting RNA, piRNAs). Despite increasing knowledge on the effects of TEs on genome evolution and the apparition of novel traits, how and which TEs along with their interactions with piRNAs can promote novelty remain unclear.
The project of Dr. Fouks will shed light on this issue by investigating how TEs and piRNAs evolved and interacted in cockroaches and termites alongside the evolution of their incredible biodiversity, with an emphasis on sociality and wood feeding.
Dr. Fouks will generate several high-resolution genomes and transcriptomes from cockroach and termite species to locate and categorize TEs and piRNAs., This will allow him to unravel their role in the adaptation of cockroaches and termites to different social levels and diets.

Controlled hydroxylations of diterpenoids allow for plant chemical defense without autotoxicity

Many plant specialized metabolites function in herbivore defense, and abrogating particular steps in their biosynthetic pathways frequently causes autotoxicity. However, the molecular mechanisms underlying their defense and autotoxicity remain unclear. Here, we show that silencing two cytochrome P450s involved in diterpene biosynthesis in the wild tobacco Nicotiana attenuata causes severe autotoxicity symptoms that result from the inhibition of sphingolipid biosynthesis by noncontrolled hydroxylated diterpene derivatives. Moreover, the diterpenes’ defensive function is achieved by inhibiting herbivore sphingolipid biosynthesis through postingestive backbone hydroxylation products. Thus, by regulating metabolic modifications, tobacco plants avoid autotoxicity and gain herbivore defense. The postdigestive duet that occurs between plants and their insect herbivores can reflect the plant’s solutions to the “toxic waste dump” problem of using potent chemical defenses.

For the full paper, please click here.


Online article on WWU news page (english)
Online article on WWU news page (german)

 

Genome Assembly and Annotation of the California Harvester Ant Pogonomyrmex californicus (Buckley, 1867)

The harvester ant genus Pogonomyrmex is endemic to arid and semiarid habitats and deserts of North and South America. The California harvester ant Pogonomyrmex californicus is the most widely distributed Pogonomyrmex species in North America. P. californicus colonies are usually monogynous, i.e. a colony has one queen. However, in a few populations in California, primary polygyny evolved, i.e. several queens cooperate in colony founding after their mating flights and continue to coexist in mature colonies. Here, we present a genome assembly and annotation of P. californicus. The size of the assembly is 241 Mb, which is in agreement with the previously estimated genome size. We were able to annotate 17,889 genes in total, including 15,688 protein-coding ones with BUSCO completeness at a 95% level. The presented P. californicus genome assembly will pave the way for investigations of the genomic underpinnings of social polymorphism in the number of queens, regulation of aggression, and the evolution of adaptations to dry habitats.

For the full paper, please click here

Jonas Bohn, Reza Halabian, Lukas Schrader, Victoria Shabardina, Raphael Steffen, Yutaka Suzuki, Ulrich R Ernst, Jürgen Gadau, Wojciech Makałowski "Genome Assembly and Annotation of the California Harvester Ant Pogonomyrmex californicus (Buckley, 1867)" (2020) G3 Genes|Genomes|Genetics

 

In October 2020, 28 pupils of Gesamtschule Münster Mitte visited the IEB (University Münster) and learned what is driving the female and male scientists. Ants, termites, proteins, computer programs – the pupils and scientists were excited- too bad there was not enough time to answer all questions! So pupils should come back soon and visit again!
 

The Institute for Evolution and Biodiversity (IEB) in the Facultyof Biology at the University of Münster, Germany, is seeking to fill apermanent position for a Scientific Staff
(einer Studienrätin/eines Studienrates im Hochschuldienst), Salary Level A13, 100%

The teaching obligation associated with this position is 13-17 (hours of instruction per weekduring semester), depending on the other general tasks assigned to the position. The weekly working time is currently 41 hours. The primarily obligations associated with the position involve teaching in the area of Zoology and Evolutionary Biology, in particular organizing and running modules for the Bachelor of Biology, Master’s of Science and Master’s of Education in German and English. The successful candidate will also be heavily involved in the statistical education of bachelor, master’s and doctoral students in the Faculty of Biology. They will also take over general tasks at the IEB according to her/his past experience. In addition to teaching, the candidate is encouraged to develop their own research program in collaboration with colleagues at the IEB and Faculty of Biology and acquire third party funding. Requirements for this position are a university degree and a doctoral degree in biology, physics, chemistry or mathematics, as well as comprehensive experience in theoretical evolutionary biology (e.g. statistical methods, modelling, etc.). To be eligible for “Beamtenverhältnis”(German civil servant status) according to § 45 LVO, the candidate needs to be able to prove employment for 3 years and 6 months after finishing her/his university degree or for 1 year after completing a doctoral degree. If the requirements are not yet fulfilled, the candidate can instead be employed as a public servant (TV-L E13) and change to the status of “Beamtenverhältnis”at a later stage. If the employee does not fulfill the requirements for a “Beamtenverhältnis” she/he can be permanently employed as a public servant (TV-L E13).
The University of Münster is an equal opportunity employer and is committed to increasing the proportion of women academics. Consequently, we actively encourage applications by women. Female candidates with equivalent qualifications and academic achievements will be preferentially considered within the framework of the legal possibilities. The University of Münster is committed to employing more staff with disabilities. Candidates with recognised severe disabilities who have equivalent qualifications are given preference in hiring decisions.

Applications including a CV, certificates of university and doctoral degrees, and details of teaching experience and publications should be sent by email as a single PDF file to evolecol@uni-muenster.de by 1 September 2020.

For the original job announcement in German please click here
 

Tiny animals with surprising characteristics

Biologist Tze Hann Ng studies how copepods react to parasites.
For more than a year now, at the University of Münster, she has been studying the mechanisms of the immune system of these tiny animals. Even before she came to Germany on a fellowship from the Humboldt Foundation, she was interested in aquatic creatures while working in her previous lab in Taiwan – although there she examined the larger “siblings”, shrimps and crayfish.

Original article in the University newspaper wissen|leben  (in German)
Online article on WWU news page


 

Since several years it is known that new proteins not only arise via gene duplication and variation of the duplicates but also de novo, i.e. from previously non-coding DNA.
An important first step in the creation of these de novo genes is that some of the zillions of randomly generated transcripts have some, though very weak, inherent function or are at least not toxic to the cell and are not quickly lost again.
In her project, Dr. Grandchamp will investigate how often new random transcripts are created, by which mechanisms they are created and what the initial function of the new proteins might be.
She plans to use in-bred lines of fly populations collected from all over Europe as well as of closely related fly species and map their transcriptomes onto the newly sequenced genomes to precisely characterise the creation and loss of de novo genes.

For Anna Grandchamp's homepage click here
For more information on the Humboldt Fellowship click here
 

Marek Golian and Nicolas Schröder successfully applied for SAFIR student research grants allowing them to pursue their own long-term research projects.
Marek will investigate the impact of surface microbes on the chemical profile of the parasitoid wasp Nasonia, while Nicolas will conduct phylogenetic and comparative genomic analyses to study the evolution of host-beneficial microbes in insects.
 

Cavefish have fewer cells of the innate immune system

Cavefish are small, live in tucked away places humans rarely go, and they’re common enough that you can find them on every continent except Antarctica. But they also have another characteristic that seems surprising at first glance: They can tell researchers something about the occurrence of autoimmune diseases in humans. Because similar to people, cavefish live in an environment with a reduced number of parasites. Unlike people, however, cavefish have had much more time – about 150,000 years – to adapt to these conditions. To learn more about how a low-parasite environment may shape the evolution of a host’s immune system, an international team of researchers led by the Stowers Institute for Medical Research examined the impact of decreased parasite abundance and infection on the evolution of the cavefish immune system.

The scientists under participation of Dr. Robert Peuß and Dr. Jörn P. Scharsack from the Institute for Evolution and Biodiversity characterized the cavefish immune system and how it responds to threats, compared to that of closely-related river fish from a parasite-rich environment. Their findings show that cavefish differ in their sensitivity toward immune stimulants and have a different composition of immune cells, including a reduction of cells of the innate immune system that play a role in inflammation.

In future studies, the scientists hope to identify genetic factors involved in cavefish immune system evolution. This research could provide clues about the development of immune system disorders and potentially human autoimmune diseases, where the immune system attacks its own body. The study has been published in the journal “Nature Ecology & Evolution”.


For the WWU press release, please click here

For the original article, please click here.

Peuß et al. (2020): Adaptation to low parasite abundance affects immune investment and immunopathological responses of cavefish. Nature Ecology & Evolution; DOI: 10.1038/s41559-020-1234-2

 

Background

Parasitoid wasps have fascinating life cycles and play an important role in trophic networks, yet little is known about their genome content and function. Parasitoids that infect aphids are an important group with the potential for biocontrol. Their success depends on adapting to develop inside aphids and overcoming both host aphid defenses and their protective endosymbionts.

Results
We present the de novo genome assemblies, detailed annotation, and comparative analysis of two closely related parasitoid wasps that target pest aphids: Aphidius ervi and Lysiphlebus fabarum (Hymenoptera: Braconidae: Aphidiinae). The genomes are small (139 and 141 Mbp), highly syntenic, and the most AT-rich reported thus far for any arthropod (GC content: 25.8% and 23.8%). This nucleotide bias is accompanied by skewed codon usage and is stronger in genes with adult-biased expression. AT-richness may be the consequence of reduced genome size, a near absence of DNA methylation, and energy efficiency. We identify missing desaturase genes, whose absence may underlie mimicry in the cuticular hydrocarbon profile of L. fabarum. We also find that absence of some immune genes (Toll and Imd pathways) resembles similar losses in their aphid hosts, highlighting the potential impact of symbiosis on both aphids and their parasitoids.


Conclusions
These findings are of fundamental interest for insect evolution and beyond. This will provide a strong foundation for further functional studies including coevolution with respect to their hosts, the basis of successful infection, and biocontrol. Both genomes are available at https://bipaa.genouest.org.


For the full paper, please click here.

Dennis, A.B., Ballesteros, G.I., Robin, S. et al. Functional insights from the GC-poor genomes of two aphid parasitoids, Aphidius ervi and Lysiphlebus fabarum. BMC Genomics 21, 376 (2020).

At a workshop orginized by the WWU "Opening Reproducible Research" (o2r) team the Evolution and Biodiversity of Plants group presented how software components can help to improve reproducibility of scientific workflows.

Here is an excerpt of an article by Dr. Ben Stöver, research group Evolution and Biodiversity of Plants (Prof. Dr. Kai Müller)

The annotation of scientific data with metadata documenting how raw data was generated and which analysis steps lead to derived data, offers an efficient way to improve the reproducibility of scientific studies. Phylogenetic trees (representing evolutionary relationships, e.g., between species) – as an example – are often inferred from DNA sequences of different species, which in turn were sequenced from tissue samples from specimens (e.g., collected plants). Ideally, a published phylogenetic tree would contain metadata that links a specific archived specimen for each species and the sequence generated from it, as well as metadata to document the analysis steps and the software used to reconstruct the tree. This principle of annotation can also be applied to other data types and can therefore be used in many areas of science.

Although file formats (e.g., NeXML) that enable appropriate annotation of trees and other phylogenetic data were developed years ago, they are still used relatively little compared to older formats that do not allow this. To change this, we at the group for Plant Evolution and Biodiversity (Prof. Dr. Kai Müller) are developing a number of different software components that make it as easy as possible for scientists to use the new file formats and the necessary annotation. At the same time, the interoperability with existing analysis software is ensured, even if it does not yet support the corresponding formats itself. Specifically, we develop graphical editors for biologists to easily process and annotate the main data types of phylogenetics, as well as, software libraries for easy reuse in other bioinformatics software. Our software is freely available at http://bioinfweb.info/.

See the full article here: https://www.uni-muenster.de/news/view.php?cmdid=10847

The German Limnological Society in cooperation with the WWU Münster invites to the freshwater conference wasser.leben.zukunft (water.life.future), taking place from 23rd-27th September 2019 at the University of Münster. Conference venue is the Fürstenberghaus. According to the motto participants will discuss current findings and future topics and global challenges we face in the field of freshwater sciences, spanning from classical limnology, organismic biology, and ecosystem ecology to innovative approaches in fundamental and applied science, accompagnied by best practice examples. Focal areas of talks and poster sessions are, among others, consequences of climate change, conservation and managing of freshwater ecosystems and biota, aquatic biodiversity, multiple stressors including neobiota, and aquatic ecotoxicology. Science communication and knowledge transfer are addressed as well. Conference language is German, yet a whole session („Zooplankton meets environmental challenges: insights from Daphnia) and various talks and posters are in English.
The side programme comprises a public evening lecture (Sept. 23th: „Climate under change !? - Satellite images show the global change“), a microscopy workshop („Leben im Aasee“) organized by Msc. Biosciences-students, a Pubquiz Special around limnological topics, organized by the Fachschaft Biologie, and various excursions in the Münsterland region at Friday, 27th. As a novelty, two Master students will maintain a Blog with daily reports, fotos etc. about the conference.

Conference homepage

In May 2019 the Institute for Evolution and Biodiversity contributed to a climate change project with the Montessori-Schule Münster e.V.. Together with the teachers Msc. student Jenny Märzhäuser of the Molecular Evolution and Sociobiology group of Prof. Jürgen Gadau organized a project concerning climate change for the older school classes as part of a research module. Therefore, differing topics on the terms climate und man-made climate change had to be worked out in groups and presented in various self-chosen ways. The students developed posters, flyers, presentations, short movies, games and even a fuel cell model car. They presented their several week-long work to the younger classes, which were eager to ask their prepared research questions about climate change. Young and old became very impressed by the importance of manmade climate change for our future and our environment through this exciting day.

Frontiers in Plant Science published a new study from Shuqing Xu’s group entitled: Evolution of alternative splicing in Eudicots. Using a machine learning approach, the authors uncovered the underlying mechanisms that contributed to the differences of alternative splicing among species.

Original publication:
Ling, Z., Brockmöller, T., Baldwin, I. T. & Xu, S. (2019). Evolution of alternative splicing in eudicots. Frontiers in Plant Science, 10, 707.; DOI: 10.3389/fpls.2019.00707