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- Plant Physiology
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Small regulatory RNAs can move between organisms and regulate gene expression in the recipient. Whether the trans-species small RNAs being exported are distinguished from the normal endogenous small RNAs of the source organism is not known. The parasitic plant Cuscuta campestris (dodder) produces many microRNAs that specifically accumulate at the host–parasite interface, several of which have trans-species activity. We found that induction of C. campestris interface-induced microRNAs is similar regardless of host species and occurs in C. campestris haustoria produced in the absence of any host. The loci-encoding C. campestris interface-induced microRNAs are distinguished by a common cis-regulatory element. This element is identical to a conserved upstream sequence element (USE) used by plant small nuclear RNA loci. The properties of the interface-induced microRNA primary transcripts strongly suggest that they are produced via U6-like transcription by RNA polymerase III. The USE promotes accumulation of interface-induced miRNAs (IIMs) in a heterologous system. This promoter element distinguishes C. campestris IIM loci from other plant small RNAs. Our data suggest that C. campestris IIMs are produced in a manner distinct from canonical miRNAs. All confirmed C. campestris microRNAs with documented trans-species activity are interface-induced and possess these features. We speculate that RNA polymerase III transcription of IIMs may allow these miRNAs to be exported to hosts.more » « less
Cuscuta spp. are obligate parasites that connect to host vascular tissue using a haustorium. In addition to water, nutrients, and metabolites, a large number of mRNAs are bidirectionally exchanged between Cuscuta spp. and their hosts. This trans-specific movement of mRNAs raises questions about whether these molecules function in the recipient species. To address the possibility that mobile mRNAs are ultimately translated, we built upon recent studies that demonstrate a role for transfer RNA (tRNA)-like structures (TLSs) in enhancing mRNA systemic movement. C. campestris was grown on Arabidopsis that expressed a β-glucuronidase (GUS) reporter transgene either alone or in GUS-tRNA fusions. Histochemical staining revealed localization in tissue of C. campestris grown on Arabidopsis with GUS-tRNA fusions, but not in C. campestris grown on Arabidopsis with GUS alone. This corresponded with detection of GUS transcripts in Cuscuta on Arabidopsis with GUS-tRNA, but not in C. campestris on Arabidopsis with GUS alone. Similar results were obtained with Arabidopsis host plants expressing the same constructs containing an endoplasmic reticulum localization signal. In C. campestris, GUS activity was localized in the companion cells or phloem parenchyma cells adjacent to sieve tubes. We conclude that host-derived GUS mRNAs are translated in C. campestris and that the TLS fusion enhances RNA mobility in the host-parasite interactions.more » « less
Moreno, Silvia N. (Ed.)ABSTRACT During their parasitic life cycle, through sandflies and vertebrate hosts, Leishmania parasites confront strikingly different environments, including abrupt changes in pH and temperature, to which they must rapidly adapt. These adaptations include alterations in Leishmania gene expression, metabolism, and morphology, allowing them to thrive as promastigotes in the sandfly and as intracellular amastigotes in the vertebrate host. A critical aspect of Leishmania metabolic adaptation to these changes is maintenance of efficient mitochondrial function in the hostile vertebrate environment. Such functions, including generation of ATP, depend upon the expression of many mitochondrial proteins, including subunits of cytochrome c oxidase (COX). Significantly, under mammalian temperature conditions, expression of Leishmania major COX subunit IV (LmCOX4) and virulence are dependent upon two copies of LACK , a gene that encodes the ribosome-associated scaffold protein, LACK ( Leishmania ortholog of RACK1 [receptor for activated C kinase]). Targeted replacement of an endogenous LACK copy with a putative ribosome-binding motif-disrupted variant (LACK R34D35G36 →LACK D34D35E36 ) resulted in thermosensitive parasites that showed diminished LmCOX4 expression, mitochondrial fitness, and replication in macrophages. Surprisingly, despite these phenotypes, LACK D34D35E36 associated with monosomes and polysomes and showed no major impairment of global protein synthesis. Collectively, these data suggest that wild-type (WT) LACK orchestrates robust LmCOX4 expression and mitochondrial fitness to ensure parasite virulence, via optimized functional interactions with the ribosome. IMPORTANCE Leishmania parasites are trypanosomatid protozoans that persist in infected human hosts to cause a spectrum of pathologies, from cutaneous and mucocutaneous manifestations to visceral leishmaniasis caused by Leishmania donovani . The latter is usually fatal if not treated. Persistence of L. major in the mammalian host depends upon maintaining gene-regulatory programs to support essential parasite metabolic functions. These include expression and assembly of mitochondrial L. major cytochrome c oxidase (LmCOX) subunits, important for Leishmania ATP production. Significantly, under mammalian conditions, WT levels of LmCOX subunits require threshold levels of the Leishmania ribosome-associated scaffold protein, LACK. Unexpectedly, we find that although disruption of LACK’s putative ribosome-binding motif does not grossly perturb ribosome association or global protein synthesis, it nonetheless impairs COX subunit expression, mitochondrial function, and virulence. Our data indicate that the quality of LACK’s interaction with Leishmania ribosomes is critical for LmCOX subunit expression and parasite mitochondrial function in the mammalian host. Collectively, these findings validate LACK’s ribosomal interactions as a potential therapeutic target.more » « less
Vigna unguiculata) cultivar B301 is resistant to races SG4 and SG3 of the root parasitic weed Striga gesnerioides, developing a hypersensitive response (HR) at the site of parasite attachment. By contrast, race SG4z overcomes B301 resistance and successfully parasitises the plant.
Comparative transcriptomics and
in silicoanalysis identified a small secreted effector protein dubbed Suppressor of Host Resistance 4z (SHR4z) in the SG4z haustorium that upon transfer to the host roots causes a loss of host immunity (i.e. decreased HR and increased parasite growth). SHR4z has significant homology to the short leucine‐rich repeat (LRR) domain of SOMATIC EMBRYOGENESIS RECEPTOR‐LIKE KINASE (SERK) family proteins and functions by binding to VuPOB1, a host BTB‐BACK domain‐containing ubiquitin E3 ligase homologue, leading to its rapid turnover.
VuPOB1 is shown to be a positive regulator of HR since silencing of VuPOB1 expression in transgenic B301 roots lowers the frequency of HR and increases the levels of successful SG4 parasitism and overexpression decreases parasitism by SG4z.
These findings provide new insights into how parasitic weeds overcome host defences and could potentially contribute to the development of novel strategies for controlling
Strigaand other parasitic weeds thereby enhancing crop productivity and food security globally.
Mistletoe spatial patterns are poorly understood on a macroecological scale. Previous research conducted at the family-level on Loranthaceae from Australia demonstrated that unlike most plants, mistletoe species richness patterns do not correlate significantly with water and energy input. However, field studies suggested a relationship between the structure of the host-parasite union (haustorium) and environment. We hypothesize that haustorial type influences relationships between the abiotic environment and mistletoe spatial patterns. To investigate this hypothesis, we constructed ecological niche models for individual haustorial types. We have previously compared the distributions of haustorial types in both geographic and environmental space using geographic mapping and PCA, respectively. Here, we expand on our study by examining species richness, constructing predictive models, and emphasizing habitat types. Using the haustorial specimen collection housed at the UC Herbarium and relevant literature, we identified the haustorial type of 55 of the 73 Australia Loranthaceae mistletoe species. Using geographic distributional data from the Atlas of Living Australia and environmental data from WorldClim, we plotted haustorial groups in both geographic and environmental space, compared clusters in principle component space, and calculated Hutchinsonian niche overlap. We used regression to analyze the relationship between species richness and environmental variables at the haustorial level. Lastly, we constructed maximum entropy models to estimate the probability of occurrence of each haustorial group, analyzing the relative contributions of each variable to each model. We discovered that haustorial type is relatively conserved among the Australian Loranthaceae mistletoe genera, with seven out of nine genera exhibiting one haustorial type. Species with epicortical roots (ER), the ancestral character, are exclusively associated with coastal regions while those with derived haustorial types occur across the continent, including desert regions. Environmental analyses confirmed that species with ER are found in regions with milder temperatures and higher precipitation than derived types. Species richness patterns of some haustorial types, including ER, are significantly correlated with most environmental variables, while derived haustorial types are not. Maxent models for species with ER haustoria predict the highest probability of occurrence for coastal regions, while models constructed for derived types feature less bias for coastal regions. Our models demonstrate that relationships between the abiotic environment and mistletoe spatial patterns depend in part on the haustorial type. Hypotheses proposed to explain relationships between abiotic constraint on distribution and haustorial type include differences in water uptake efficiency, exposure of haustoria to the environment, longevity of haustoria, and host preference of species.more » « less