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Wicke, S.

Publications and source records attributed to Wicke, S..

14 recordsLinked to original sources

Systemic organellar genome reconfiguration along the parasitic continuum in the Broomrape family (Orobanchaceae)

The transition from autotrophy to heterotrophy in parasitic plants disrupts organellar coordination and presents a unique opportunity to examine the coevolution of cellular genomes. Using the Broomrape family (Orobanchaceae) as a model, we analyzed mitochondrial and plastid genome evolution across 30 species representing the full spectrum of parasitic lifestyles. We show that plastid genome reduction is correlated with mitogenomic expansion, revealing a striking inverse relationship between genome compaction and inflation. Mitogenome enlargement in parasitic taxa is driven by the accumulation of horizontally and intracellularly transferred DNA, proliferation of short repeats, and integration of unique sequences with no detectable homology. Notably, foreign DNA insertions converge toward native mitochondrial GC content and often retain structural functionality, suggesting selective maintenance. Relaxed selection in ATP synthase and ribosomal genes contrasts with intensified selection on components of electron transport and cytochrome c maturation, reflecting functional reconfiguration of mitochondrial respiration in parasitic plants. RNA editing, intron loss, and frameshift insertions further reshape gene structure, particularly in obligate parasites. Together, our findings suggest that parasitism initiates a systemic genomic feedback loop in which relaxed selection and disrupted maintenance mechanisms affect even distant genomic compartments. This study provides the first comprehensive evolutionary framework for multi-compartment genome remodeling in parasitic plants and highlights the dynamic interplay between lifestyle specialization and organelle genome evolution.

evolutionary biology↗

Submersion and oxidative stress triggers pyrenoid formation, carbon concentration-related protein remodeling and sub-plastidial rearrangements in hornworts

Plastids are important for controlling acclimation of plants to environmental changes. In hornworts, chloroplasts may contain a RuBisCO-enriched protein matrix, a pyrenoid-like structure, which enables them to perform a biophysical carbon concentration mechanism (CCM) at the single-cell level- a unique feature among land plants. However, much remains unknown about the function, formation, and regulation of hornwort pyrenoids, especially as they are unaffected by changes in atmospheric CO2. Here, we tested whether submersion and hyperoxia induce pyrenoid formation and CCM. By subjecting Anthoceros agrestis, a pyrenoid-forming hornwort species, and A. fusiformis, which develops no pyrenoids, to a series of submersion experiments and analyzing their molecular, physiological, and cell-morphological response patterns using label-free proteomics and transmission electron microscopy, with additional in silico analysis, we identified a core set of CCM candidate genes. Under submersion, both species expressed CCM-associated protein homologs, whereas hyperoxia induced or diminished the expression of CCM-like homologs in a species-specific manner. We discovered that a carbonic anhydrase, a CAH3 homolog, as well as thylakoid bicarbonate transporter (LCI11-like) are upregulated under both conditions in A. agrestis, but not in A. fusiformis, suggesting that an algae-like mechanism of bicarbonate pumping into the thylakoid lumen and CO2 conversion exists in A. agrestis. Corroborating these molecular findings, an ultrastructural analysis of plastids revealed increases in pyrenoid-like structures and rearrangements during submersion in A. agrestis, whereas A. fusiformis accumulated lipid droplets between thylakoid stacks. Together, our data highlight hornworts distinct acclimation strategies to adverse environmental conditions, highlighting the relevance of their pyrenoids and CCM. Significance statementCarbon concentration via pyrenoids, densely packed matrices of a CO2-fixing enzyme, holds significant biotechnological promise for enhancing crop resilience. Studying mechanisms underlying pyrenoid formation in hornworts--the only land plants to naturally develop pyrenoids--is of exceptional interest due to their evolutionary closeness to crops. This study closes a knowledge gap by showing that hornworts use pyrenoids and a carbon-concentrating mechanism to adapt to submersion and hyperoxia, allowing them to thrive under regular transitions between atmospheric and submerged environments, resembling conditions during plants water-to-land transition. Species lacking pyrenoids accumulate lipid droplets instead, in addition to altering developmental and physiological pathways. Together, this work highlights hornworts remarkable versatility and untapped potential in advancing our understanding of plant adaptation to terrestrial life.

plant biology↗

Molecular underpinnings of hornwort carbon concentrating mechanisms: subcellular localization of putative key molecular components in the model hornwort Anthoceros agrestis.

O_LIBiophysical carbon concentrating mechanisms (CCMs) operating at the single-cell level have evolved independently in eukaryotic algae and a single land plant lineage, hornworts. An essential component for an efficient eukaryotic CCM is a pyrenoid whose biology is well-characterized in the unicellular green alga, Chlamydomonas reinhardtii. By contrast, pyrenoids and CCM are little understood in hornworts. C_LIO_LIHere, we investigate the molecular underpinnings and dynamics of hornwort pyrenoids. We do so by studying the subcellular localization of candidate proteins homologous to essential CCM genes in C. reinhardtii and assessing their mobility kinetics in the hornwort model Anthoceros agrestis. C_LIO_LIWe provide evidence that an EPYC1 analog and the RuBisCO co-localize in the pyrenoid but pyrenoids seem less dynamic in A. agrestis than in C. reinhardtii. We further found that a carbon anhydrase homolog (CAH3) localizes to the pyrenoid, while an LCIB-like homolog is less intimately linked to the pyrenoid than in C. reinhardtii. C_LIO_LIOur results imply that the pyrenoid-based CCM of hornworts is characterized by a mixture of Chlamydomonas-like as well as hornwort-specific features which is in line with its independent evolutionary origin. Using these observations, we provide a first mechanistic model of hornwort CCM. C_LI

plant biology↗

Acclimation kinetics of the holoparasitic weed Phelipanche ramosa (Orobanchaceae) during excessive light and heat conditions

Holoparasitic plants, such as broomrape, have abandoned a photosynthesis, relying entirely on the resources of host plants. This departure from an autotrophic lifestyle necessitates significant genetic and metabolic adaptations, offering a unique model system to elucidate responses independent of canonical plastid functions in green plants. In this study, we examined the acclimation kinetics of the holoparasitic weed Phelipanche ramosa (broomrape) under unfavorable temperature and excessive light conditions through a comprehensive time-course analysis of RNA sequence data and physiological monitoring. Our work unveils that suboptimal abiotic conditions induce transcriptional changes in the parasitic plant, involving coordinated expression of nuclear and plastid-encoded genes. Notably, magnesium transporters, critical for heat-induced chlorophyll conversion, were enriched among heat-repressed genes. Additionally, multiple copies of chloroplast-targeted DnaJ proteins, responsible for maintaining CO2 assimilation capacity in non-parasitic plants, were identified. Comparative expression analysis with the parasites host plants, tomato and Arabidopsis, revealed distinct patterns for certain plastid genes in Phelipanche. Furthermore, an elevation in reactive oxygen species (ROS) in the parasite coincided with the upregulation of numerous heat shock protein (HSP) genes, including HSP21, which associates with thylakoid membranes in photosynthetic plants; noteworthily, thylakoids are absent from Phelipanches plastids. Collectively, our findings suggest that plastids of the nonphotosynthetic model plant retains their ancestral role as environmental sensors. This research opens new avenues for functional-genetic research into the nuanced roles of plastids in the lifecycles of parasitic plants.

plant biology↗

Ribosomal Incorporation of Short RNAs from Mitochondrial Genome Recombination Sites in Toxoplasma gondii

The mitochondrial genomes of apicomplexans comprise merely three protein-coding genes, alongside a set of thirty to forty genes encoding small RNAs (sRNAs), many of which exhibit homologies to rRNA from E. coli. The expression status and integration of these short RNAs into ribosomes remains unclear and direct evidence for active ribosomes within apicomplexan mitochondria is still lacking. In this study, we conducted small RNA sequencing on the apicomplexan Toxoplasma gondii to investigate the occurrence and function of mitochondrial sRNAs. To enhance the analysis of sRNA sequencing outcomes, we also re-sequenced the T. gondii mitochondrial genome using an improved organelle enrichment protocol and Nanopore sequencing. It has been established previously that the T. gondii genome comprises 21 sequence blocks that undergo recombination among themselves but that their order is not entirely random. The enhanced coverage of the mitochondrial genome allowed us to characterize block combinations at increased resolution. Employing this refined genome for sRNA mapping, we find that many small RNAs originated from the junction sites between protein-coding blocks and rRNA sequence blocks. Surprisingly, such block border sRNAs were incorporated into polysomes together with canonical rRNA fragments and mRNAs. In conclusion, apicomplexan ribosomes are active within polysomes and are indeed assembled through the integration of sRNAs, including previously undetected sRNAs with merged mRNA-rRNA sequences. Our findings lead to the hypothesis that T. gondiis block-based genome organization enables the dual utilization of mitochondrial sequences as both messenger RNAs and ribosomal RNAs, potentially establishing a link between the regulation of rRNA and mRNA expression.

molecular biology↗

Comparative gene expression analysis of differentiated terminal and lateral haustoria of the obligate root parasitic plant Phelipanche ramosa (Orobanchaceae)

AO_SCPLOWBSTRACTC_SCPLOWBranched broomrape (Phelipanche ramosa, Orobanchaceae) is the most important parasitic weed of oilseed and vegetable crops in Europe. Deciphering the parasites basic biology and genetics underpinning adaptations to parasitism are essential for effective weed management. Here, we compared the gene expression profiles of differentiated terminal haustoria, formed immediately after the germination of P. ramosa with those of the parasites adventitious roots and lateral haustoria, which develop on the latter as it grows. Principal component analysis and functional annotation of differentially expressed genes indicate a greater transcriptional similarity between adventitious roots and lateral haustoria compared to terminal haustoria. Genes involved in hydrogen peroxide catabolic processes and mucilage metabolic processes were more abundant in lateral haustoria compared to adventitious roots, indicating that secondary host attachment involves secretion of adhesive compounds, cell wall modification, and a termination of the developmental program associated with root growth. In terminal haustoria, phytohormonal signaling pathways for post-germination growth and meristem development were the most prominent expression profile difference to lateral haustoria. Besides this, wide similarity of expressed genes between lateral and terminal haustoria suggest overlapping pathways underlying haustorium differentiation and a conserved functional relevance of both haustoria types at maturity. Together, our study provides first insights into the transcriptional landscapes of the primary organs securing P.ramosas nutritional success. However, more research is needed to investigate whether the parasites various haustorium types differ in their sensitivities to environmental stimuli and whether transcriptional divergence in terminal and lateral haustoria of P. ramosa reflect differences regarding their developmental origin.

plant biology↗

Aging seeds of weedy broomrapes and witchweeds lose sensitivity to strigolactones as DNA demethylates

Broomrapes (Phelipanche and Orobanche spp.) and witchweeds (Striga and Alectra spp.) are obligate root parasitic weeds responsible for major crop yield losses worldwide. Their success in agricultural landscapes is attributable to their ability to produce thousands of long-lived minute seeds that coordinate their germination with the presence of nearby hosts by perceiving host-derived strigolactones. Nevertheless, the processes underlying the alleged decade(s)-long persistence in the field are understudied. Using an accelerated seed aging method coupled to germination and ELISA bioassays, we report that the loss of seed viability and germinability along seed aging is accompanied by a decrease in both strigolactone sensitivity and global DNA methylation. Our results also suggest that seeds of broomrapes are longer-lived than those of witchweeds. Overall, this study deems to initiate further research into how epigenetic mechanisms contribute to alterations in seed viability in parasitic weeds, and how seed aging influence seed responses to their environment.

plant biology↗

New mitochondrial genomes of leptosporangiate ferns allow modeling the mitogenomic inflation syndrome across all land plant lineages

Plants mitochondrial genomes (mitogenome) evolve in a hard-to-predict fashion. To reconstruct the evolutionary trajectories of land plant mitogenomes, we, here, filled the last major mitogenomic gap within land plants by assembling the mitogenomes of the leptosporangiate ferns Azolla filiculoides and Pteridium revolutum and, secondly, analyzed the mitogenomic evolutionary regime shifts across land plants. By testing various Ornstein-Uhlenbeck stabilizing selection models in an a priori-free analysis of five selected mitogenomic traits, we observed 71 evolutionary regime shifts across 218 land plant species. These shifts can lead to genomic convergence, in which certain traits such as size, GC content, and the proportion of non-coding DNA converge, or non-converging regimes, which are characterized by exceptional paths of genomic evolution such as extreme GC content or size. We also found that non-seed plants have a slightly, but significantly, higher rate of synonymous substitutions across all gene classes than seed plants, and that ferns differ significantly in the number of nonsynonymous and synonymous changes compared with other non-seed and seed plants. This pattern matches an outstandingly high rate of RNA editing in the small but repeat-rich mitogenomes of leptosporangiate ferns. In sum, our study highlights the considerable changes in mito-chromosomal architecture that occur during land plant evolution and suggests that these changes may be related to increases in error-prone repair mechanisms. Further study of underrepresented plant groups such as ferns and lycophytes is needed to understand the mechanisms and dominating forces behind the evolutionary dynamics and the mitogenomic inflation syndrome. Significance StatementOur study provides new insights into the complexity and diversity of land plant mitogenome evolution and reveals that they take many turns of molecular evolutionary directions across 218 land plant species. Our results have the potential to inform future research in this area and to advance our understanding of the mitogenomic inflation syndrome during plant evolution.

evolutionary biology↗

Gene complementation analysis suggests that dodder plants (Cuscuta spp.) do not depend on the host FT protein for flowering

Dodder (Cuscuta spp.) is a genus of parasitic plants that form physiological bridges (haustoria) with their hosts to facilitate the transfer of water and nutrients. The parasites also repurpose nucleic acids and proteins translocating through the haustoria, potentially including the host florigen protein (FT), which is postulated to trigger floral transition in the parasite. Here, we identified the endogenous FT-FD flowering module in Cuscuta campestris. We detected the expression of two parasite-encoded C. campestris (Cc)FT genes in haustoria, whereas a newly found CcFD-like gene was expressed ubiquitously. C. campestris flowered while growing on mutant tobacco plants lacking the floral activators NtFT4 and NtFT5, indicating that host FT proteins are not required to initiate the parasites floral transition. We also showed that CcFT1 (identical to CaFT from Cuscuta australis) and CcFT2 can rescue a non-flowering Ntft4-Ntft5- double knockout tobacco phenotype. Together, our results show that Cuscuta spp. produce a potent endogenous florigen as well as other proteins likely to be involved in floral transition. FT gene expression profiles in the haustoria suggest that Cuscuta spp. transition to flowering at least partly in response to host signals (e.g., sugars) that can activate the parasites FT-FD module. Although C. campestris and C. australis appear not to depend on the host FT protein for floral transition, the nature of the mobile host signals that influence floral development in these parasites remain unclear. Significance StatementParasitic higher plants are known for their sophisticated adaptations that facilitate the transfer of water and nutrients from their hosts. They can also synchronize their transition from vegetative to reproductive development to match the host plant. Despite this high degree of synchronization, dodder plants maintain a potent endogenous floral activator module, which enables the parasite to switch to reproductive development autonomously. Synchronization must therefore involve other stimuli from the host plant, which are currently unknown. Understanding the environmental cues that trigger flowering, and the corresponding network of genetic and physiological regulators and integrators, may lead to new strategies that reduce the reproductive fitness of parasitic plants to protect crops and ensure food security. Data ServersThis article is available as preprint (ID: BIORXIV/2022/520981) at https://www.biorxiv.org under the CC BY-NC 4.0 license. Reusable data files have been deposited at https://datadryad.org, accessible during peer-review under: https://datadryad.org/stash/share/DK8Olh2VqFwbGNL0GtkGt24dD0GhWhJn82oLBC1XK70

plant biology↗

A transcriptome atlas of Striga hermonthica germination

Societal Impact StatementWitchweeds, parasitic plants of the genus Striga, are nicknamed "cereal killers" because of their devasting destruction of Africas most staple cereals, including maize, sorghum, millets, and upland rice. The parasite relies on biomolecules emitted from the host roots to germinate and therefore initiate its infectious lifecycle. Some sorghum varieties have evolved to not produce effective germination stimulants, making them resistant to the parasite. Here, we assess genetic factors that underpin Striga germination. We discuss how such knowledge can be used to develop new Striga management strategies through the disruption of host-parasite communication exchange. SummaryO_LISeeds of the parasitic plant Striga are dormant. They only germinate in response to biomolecules emitted from the hosts root exudate, strigolactones (SL). But, it is now emerging that Striga germination is a much more complex process regulated by crosstalk of hormone signaling pathways. C_LIO_LITo further understand the genetic basis of the communication exchange between Striga and its host sorghum, we performed a comparative transcriptomic analysis. We sought to identify major transcriptomic changes that define the germination process in Striga and a set of genes that may contribute to the differences in germination rates. C_LIO_LIResults showed that germination proceeds immediately after SL perception and is marked by a wave of transcriptional reprogramming to allow for metabolic processes of energy mobilization. Cluster analysis using self-organizing maps (SOMs) revealed a time-phased and genotype-differentiated response to germination stimulation. The variation in germination was also a function of hormonal crosstalk. The early germination stage was associated with significant repression of genes in the abscisic acid (ABA) biosynthesis pathway. Other hormones influenced germination as follows: (i) ABA and auxin repressed germination, (ii) brassinosteroid, ethylene and jasmonic acid promoted germination, and (iii) cytokinin had a more prominent role post-germination rather than during germination. Perception of SL sets the germination programme leading to different rates of germination in sorghum followed by a complex hormonal regulation network that acts to either repress or enhance germination. These results have far-reaching implications for developing Striga management strategies by disrupting hormonal communication exchange. C_LI

plant biology↗

Resolving intergenotypic Striga resistance in sorghum

Genetic underpinnings of host-pathogen interactions in the parasitic plant Striga hermonthica,a root parasitic plant that ravages cereals in sub-Saharan Africa, are unclear. We performed a comparative transcriptome study on five genotypes of sorghum exhibiting diverse resistance responses to S. hermonthica using weighted gene co-expression network analysis (WGCNA). We found that S. hermonthica elicits both basal and effector-triggered immunity - like a bona fide pathogen. Resistance response was genotype-specific. Some resistance responses followed the salicylic acid-dependent signaling pathway for systemic acquired resistance characterized by cell wall reinforcements, lignification and callose deposition while in others the WRKY-dependent signaling pathway was activated leading to a hypersensitive response (HR). In some genotypes, both modes of resistance were activated while in others, either mode dominated the resistance response. Cell-wall-based resistance was common to all sorghum genotypes but strongest in IS2814, while HR-based response was specific to N13, IS9830 and IS41724. WGCNA further allowed for pinpointing of S. hermonthica resistance causative genes in sorghum. Some highlights include a Glucan synthase-like 10, a pathogenesis-related thaumatin-like family, and a phosphoinositide phosphatase gene. Such candidate genes will form a good basis for subsequent functional validation and possibly future resistance breeding. HighlightParasitic plants of the Striga genus are major pests to cereals in Africa. We pinpointed genetic causes of Striga resistance in sorghum that can be harnessed for future resistance breeding.

plant biology↗

Genomic signatures of host-specific selection in a parasitic plant

PremiseParasitic plants and their hosts are model systems for studying genetic variation in species interactions across environments. The parasitic plant Striga hermonthica (witchweed) attacks a range of cereal crop hosts in Africa and exhibits substantial variation in performance on different host species. Some of this variation is due to local adaptation, but the genetic basis of specialization on certain hosts is unknown. MethodsTo identify genomic regions that are strongly differentiated between parasites attacking different host species, we present an alignment-free analysis of S. hermonthica population diversity using whole genome sequencing (WGS) data for 68 individuals from western Kenya. We validate our findings with germination experiments and analyses based on a de novo assembled draft genome. ResultsReference-free and reference-based analyses suggest that only a small portion of the S. hermonthica genome is strongly differentiated by host species in populations from western Kenya. Analysis of host-associated k-mers implicated genes involved in development of the parasite haustorium (a specialized structure used to establish vascular connections with host roots) and a potential role of chemocyanins in molecular host-parasitic plant interactions. Conversely, no phenotypic or genomic evidence was observed suggesting host-specific selection on parasite response to strigolactones, hormones exuded by host roots and required for parasite germination. ConclusionsThis study demonstrates the utility of WGS for plant species with large, complex genomes and no available reference. Contrasting with theory emphasizing the role of early recognition loci for host specificity, our findings support host-specific selection on later interaction stages, recurring each generation after homogenizing gene flow.

evolutionary biology↗

A Phelipanche ramosa KAI2 Protein Perceives enzymatically Strigolactones and Isothiocyanates

Phelipanche ramosa is an obligate root-parasitic weed threatening major crops in central Europe. For its germination, it has to perceive various structurally diverging host-exuded signals, including isothiocyanates (ITCs) and strigolactones (SLs). However, the receptors involved are still uncharacterized. Here, we identified five putative SL receptors in P. ramosa, of which PrKAI2d3 is involved in seed germination stimulation. We established the high plasticity of PrKAI2d3, allowing interaction with different chemicals, including ITCs. The SL perception mechanism of PrKAI2d3 is similar to that of endogenous SLs in non-parasitic plants. We provide evidence that the PrKAI2d3 enzymatic activity confers hypersensitivity to SLs. Additionally, we demonstrated that methylbutenolide-OH binds PrKAI2d3 and stimulates P. ramosa germination with a bioactivity comparable to that of ITCs. This study highlights that P. ramosa has extended its signal perception system during evolution, a fact to be considered in the development of specific and efficient biocontrol methods.

plant biology↗

Morphology, geographic distribution, and host preferences are poor predictors of phylogenetic relatedness in the mistletoe genus Viscum L.

Besides their alleged therapeutic effects, mistletoes of the genus Viscum L. (Viscaceae) are keystone species in many ecosystems across Europe, Africa, Asia and Australia because of their complex faunal interactions. We here reconstructed the evolutionary history of Viscum based on plastid and nuclear DNA sequence data. We obtained a highly resolved phylogenetic tree with ten well-supported clades, which we used to understand the spatio-temporal evolution of these aerial parasites and evaluate the contribution of reproductive switches and shifts in host ranges to their distribution and diversification. The genus Viscum originated in the early Eocene in Africa and appeared to have diversified mainly through geographic isolation, in several cases apparently coinciding with shifts in host preferences. During its evolution, switches in the reproductive mode from ancestral dioecy to monoecy imply an important role in the long-distance dispersal of the parasites from Africa to continental Asia and Australia. We also observed multiple cases of photosynthetic surface reduction (evolution of scale leaves) within the genus, probably indicative of increasing specialization associated with the parasitic lifestyle. Even compared with other parasitic angiosperms, where more host generalists than specialists exist, Viscum species are characterized by extraordinarily broad host ranges. Specialization on only a few hosts from a single family or order occurs rarely and is restricted mostly to very recently evolved lineages. The latter mostly derive from or are closely related to generalist parasites, implying that niche shifting to a new host represents an at least temporary evolutionary advantage in Viscum.

evolutionary biology↗