Novel Approaches for Species Concepts and Delimitation in Polyploids and Hybrids

Hybridization and polyploidization are important processes for plant evolution. However, classification of hybrid or polyploid species has been notoriously difficult because of the complexity of processes and different evolutionary scenarios that do not fit with classical species concepts. Polyploid complexes are formed via combinations of allopolyploidy, autopolyploidy and homoploid hybridization with persisting sexual reproduction, resulting in many discrete lineages that have been classified as species. Polyploid complexes with facultative apomixis result in complicated net-work like clusters, or rarely in agamospecies. Various case studies illustrate the problems that apply to traditional species concepts to hybrids and polyploids. Conceptual progress can be made if lineage formation is accepted as an inevitable consequence of meiotic sex, which is established already in the first eukaryotes as a DNA restoration tool. The turnaround of the viewpoint that sex forms species as lineages helps to overcome traditional thinking of species as “units”. Lineage formation and self-sustainability is the prerequisite for speciation and can also be applied to hybrids and polyploids. Species delimitation is aided by the improved recognition of lineages via various novel -omics methods, by understanding meiosis functions, and by recognizing functional phenotypes by considering morphological-physiological-ecological adaptations.

The legacy of the extinct Neotropical megafauna on plants and biomes

Large mammal herbivores are important drivers of plant evolution and vegetation patterns, but the extent to which plant trait and ecosystem geography currently reflect the historical distribution of extinct megafauna is unknown. We address this question for South and Central America (Neotropical biogeographic realm) by compiling data on plant defence traits, climate, soil, and fire, as well as on the historical distribution of extinct megafauna and extant mammal herbivores. We show that historical mammal herbivory, especially by extinct megafauna, and soil fertility explain substantial variability in wood density, leaf size, spines and latex. We also identified three distinct regions (‘‘antiherbiomes’’), differing in plant defences, environmental conditions, and megafauna history. These patterns largely matched those observed in African ecosystems, where abundant megafauna still roams, and suggest that some ecoregions experienced savanna-to-forest shifts following megafauna extinctions. Here, we show that extinct megafauna left a significant imprint on current ecosystem biogeography.

Plant speciation in the Namib Desert: origin of a widespread derivative species from a narrow endemic

Background: Parapatric (or budding) speciation is increasingly recognized as an important phenomenon in plant evolution but its role in extreme (e.g. desert) environments is poorly documented. Aims: To test this speciation model in a hypothesized sister pair, the Southwest and North African disjunct Senecio flavus and its putative progenitor, the Namibian Desert endemic S. englerianus. Methods: Phylogenetic inferences were combined with niche divergence tests, morphometrics, and experimental genetic approaches. We also evaluated the potential role of an African Dry Corridor (ADC) in promoting the hypothesized northward expansion of S. flavus (from Namibia), using palaeodistribution models. Results: Belonging to an isolated (potentially relict) clade, the two morphologically distinct species show pronounced niche divergence in Namibia and signs of digenic epistatic hybrid incompatibility (based on F2 pollen fertility). The presence of connate fluked pappus hairs in S. flavus, likely increasing dispersal ability, is controlled by a single gene locus. Conclusions: Our results provide support for a rare example of budding speciation in which a wider ranged derivative (S. flavus) originated at the periphery of a smaller ranged progenitor (S. englerianus) in the Namib Desert region. The Southwest and North African disjunction of S. flavus could have been established by dispersal across intermediate ADC areas during periods of (Late) Pleistocene aridification.

Functional Analyses of the Two Distinctive Types of Two-Pore Channels (TPCs) and the Slow Vacuolar Channel in Marchantia polymorpha

The two-pore channel (TPC) family is widely conserved in eukaryotes. Many vascular plants, including Arabidopsis and rice, possess a single TPC gene which functions as a slow vacuolar (SV) channel—voltage-dependent cation-permeable channel located in the vacuolar membrane (tonoplast). On the other hand, a liverwort Marchantia polymorpha genome encodes three TPC homologs: MpTPC1 is similar to TPCs in vascular plants (type 1 TPC), while MpTPC2 and MpTPC3 are classified into a distinctive group (type 2 TPC). Phylogenetic analysis suggested that the type 2 TPC emerged before the land colonization in plant evolution and was lost in vascular plants and hornworts. All of the three MpTPCs were shown to be localized at the tonoplast. We generated knockout mutants of tpc1, tpc2, tpc3, and tpc2 tpc3 double mutant by CRISPR/Cas9 genome editing and performed patch-clamp analyses of isolated vacuoles. The SV channel activity was abolished in the Mptpc1 loss-of-function mutant (Mptpc1-1KO), while Mptpc2-1KO, Mptpc3-1KO, and Mptpc2-2/tpc3-2KO double mutant exhibited similar activity to the wild type, indicating that MpTPC1 (type 1) is solely responsible for the SV channel activity. Activators of mammalian TPC channels, PI(3,5)P2, and, NAADP, did not affect the ion channel activity of any MpTPCs. These results indicate that the type 1 TPCs, which are well conserved in all land plant species, encode the SV channel, while the type 2 TPCs likely encode other tonoplast cation channel(s) distinct from the SV channel and animal TPC channels.

DNA methylation in transposable elements disrupts the connection between three-dimensional chromatin organization and gene expression upon rice genome duplication.

Polyploidy serves as a major force in plant evolution and domestication of cultivated crops. However, the relationship and underlying mechanism between three-dimensional (3D) chromatin organization and gene expression upon rice genome duplication is largely unknown. Here we compared the 3D chromatin structures between diploid (2C) and autotetraploid (4C) rice by high-throughput chromosome conformation capture analysis, and found that 4C rice presents weakened intra-chromosomal interactions compared to its 2C progenitor. Moreover, we found that changes of 3D chromatin organizations including chromatin compartments, topologically associating domain (TAD) and loops uncouple from gene expression. Moreover, DNA methylations in the regulatory sequences of genes in compartment A/B switched regions and TAD boundaries are not related to their expressions. Importantly, in contrast to that there was no significant difference of methylation levels in TEs in promoters of differentially expressed genes (DEGs) and non-DEGs between 2C and 4C rice, we found that the hypermethylated transposable elements across genes in compartment A/B switched regions and TAD boundaries suppress the expression of these genes. We propose that the rice genome doubling might modulate TE methylation which results in the disconnection between the alteration of 3D chromatin structure and gene expression.

Cytokinin Perception in Ancient Plants beyond Angiospermae

Cytokinins (CKs) control many plant developmental processes and responses to environmental cues. Although the CK signaling is well understood, we are only beginning to decipher its evolution. Here, we investigated the CK perception apparatus in early-divergent plant species such as bryophyte Physcomitrium patens, lycophyte Selaginella moellendorffii, and gymnosperm Picea abies. Of the eight CHASE-domain containing histidine kinases (CHKs) examined, two CHKs, PpCHK3 and PpCHK4, did not bind CKs. All other CHK receptors showed high-affinity CK binding (KD of nM range), with a strong preference for isopentenyladenine over other CK nucleobases in the moss and for trans-zeatin over cis-zeatin in the gymnosperm. The pH dependences of CK binding for these six CHKs showed a wide range, which may indicate different subcellular localization of these receptors at either the plasma- or endoplasmic reticulum membrane. Thus, the properties of the whole CK perception apparatuses in early-divergent lineages were demonstrated. Data show that during land plant evolution there was a diversification of the ligand specificity of various CHKs, in particular, the rise in preference for trans-zeatin over cis-zeatin, which indicates a steadily increasing specialization of receptors to various CKs. Finally, this distinct preference of individual receptors to different CK versions culminated in vascular plants, especially angiosperms.

Case not closed: the mystery of the origin of the carpel

The carpel is a fascinating structure that plays a critical role in flowering plant reproduction and contributed greatly to the evolutionary success and diversification of flowering plants. The remarkable feature of the carpel is that it is a closed structure that envelopes the ovules and after fertilization develops into the fruit which protects, helps disperse, and supports seed development into a new plant. Nearly all plant-based foods are either derived from a flowering plant or are a direct product of the carpel. Given its importance it’s no surprise that plant and evolutionary biologists have been trying to explain the origin of the carpel for a long time. Before carpel evolution seeds were produced on open leaf-like structures that are exposed to the environment. When the carpel evolved in the stem lineage of flowering plants, seeds became protected within its closed structure. The evolutionary transition from that open precursor to the closed carpel remains one of the greatest mysteries of plant evolution. In recent years, we have begun to complete a picture of what the first carpels might have looked like. On the other hand, there are still many gaps in our understanding of what the precursor of the carpel looked like and what changes to its developmental mechanisms allowed for this evolutionary transition. This review aims to present an overview of existing theories of carpel evolution with a particular emphasis on those that account for the structures that preceded the carpel and/or present testable developmental hypotheses. In the second part insights from the development and evolution of diverse plant organs are gathered to build a developmental hypothesis for the evolutionary transition from a hypothesized laminar open structure to the closed structure of the carpel.

An ancient antimicrobial protein co-opted by a fungal plant pathogen for in planta mycobiome manipulation

Microbes typically secrete a plethora of molecules to promote niche colonization. Soil-dwelling microbes are well-known producers of antimicrobials that are exploited to outcompete microbial coinhabitants. Also, plant pathogenic microbes secrete a diversity of molecules into their environment for niche establishment. Upon plant colonization, microbial pathogens secrete so-called effector proteins that promote disease development. While such effectors are typically considered to exclusively act through direct host manipulation, we recently reported that the soil-borne, fungal, xylem-colonizing vascular wilt pathogen Verticillium dahliae exploits effector proteins with antibacterial properties to promote host colonization through the manipulation of beneficial host microbiota. Since fungal evolution preceded land plant evolution, we now speculate that a subset of the pathogen effectors involved in host microbiota manipulation evolved from ancient antimicrobial proteins of terrestrial fungal ancestors that served in microbial competition prior to the evolution of plant pathogenicity. Here, we show that V. dahliae has co-opted an ancient antimicrobial protein as effector, named VdAMP3, for mycobiome manipulation in planta. We show that VdAMP3 is specifically expressed to ward off fungal niche competitors during resting structure formation in senescing mesophyll tissues. Our findings indicate that effector-mediated microbiome manipulation by plant pathogenic microbes extends beyond bacteria and also concerns eukaryotic members of the plant microbiome. Finally, we demonstrate that fungal pathogens can exploit plant microbiome-manipulating effectors in a life stage–specific manner and that a subset of these effectors has evolved from ancient antimicrobial proteins of fungal ancestors that likely originally functioned in manipulation of terrestrial biota.

Molecular Network for Regulation of Ovule Number in Plants

In seed-bearing plants, the ovule (“small egg”) is the organ within the gynoecium that develops into a seed after fertilization. The gynoecium located in the inner compartment of the flower turns into a fruit. The number of ovules in the ovary determines the upper limit or the potential of seed number per fruit in plants, greatly affecting the final seed yield. Ovule number is an important adaptive characteristics for plant evolution and an agronomic trait for crop improvement. Therefore, understanding the mechanism and pathways of ovule number regulation becomes a significant research aspect in plant science. This review summarizes the ovule number regulators and their regulatory mechanisms and pathways. Specially, we construct the first integrated molecular network for ovule number regulation, in which phytohormones played a central role, followed by transcription factors, enzymes, other protein and micro-RNA. Of them, AUX, BR and CK are positive regulator of ovule number, whereas GA acts negatively on it. Interestingly, many ovule number regulators have conserved functions across several plant taxa, which should be the targets of genetic improvement via breeding or gene editing. Many ovule number regulators identified to date are involved in the diverse biological process, such as ovule primordia formation, ovule initiation, patterning, and morphogenesis. The relations between ovule number and related characteristics/traits especially of gynoecium/fruit size, ovule fertility, and final seed number, as well as upcoming research questions, are also discussed. In summary, this review provides a general overview of the present finding in ovule number regulation, which represents a more comprehensive and further cognition on it.