Genomics of Parasitic Plants: History
View Latest Version
Please note this is an old version of this entry, which may differ significantly from the current revision.
Contributor:
Vasily V. Ashapkin
,
Lyudmila I. Kutueva
,
Nadezhda I. Aleksandrushkina
,
Boris F. Vanyushin
,
Denitsa R. Teofanova
,
Lyuben I. Zagorchev

Parasitic plants extract nutrients from the other plants to finish their life cycle and reproduce. The control of parasitic weeds is notoriously difficult due to their tight physical association and their close biological relationship to their hosts. Parasitic plants differ in their susceptible host ranges, and the host species differ in their susceptibility to parasitic plants. Data show that adaptations of parasitic plants to various hosts are largely genetically determined. However, multiple cases of rapid adaptation in genetically homogenous parasitic weed populations to new hosts strongly suggest the involvement of epigenetic mechanisms. Progress in genome-wide analyses of gene expression and epigenetic features revealed many new molecular details of the parasitic plants’ interactions with their host plants.

  • parasitic plants
  • host plants
  • haustorium
  • genomics
  • transcriptomics

1. Striga

The sequenced genome of Striga asiatica was predicted to contain 34,577 genes and retained evidence of at least two whole-genome duplication events as well as some gene losses and gains compared with most photosynthetic plants [1]. By comparing it to the lists of the haustorium gene orthogroups [2] and genes with tissue-specific expression in Arabidopsis thaliana, a significant enrichment for tissue-specific orthogroups was found in the S. asiatica haustorial genes. In accordance with Yang et al. [2], this pattern was strongest for pollen orthogroups. Thus, evolutionary gain of a haustorium might occur through co-option of genes with tissue-specific gene expression. Relative to common ancestors of S. asiatica and its closely related non-parasitic plant Mimulus guttatus, ~23% of 10,248 orthogroups showed changes in gene numbers in the Striga lineage (647 contractions, 1742 expansions, 456 losses, and 152 gains). The relative age of genes in contracted orthogroups was significantly older than genes in expanded families. Moreover, the expanded gene families showed higher ratios of non-synonymous to synonymous substitutions compared with the contracted gene families. Thus, relatively younger expanded gene families evolved under more relaxed selection pressure, at least at the earlier stages of their evolution, potentially providing a source of genes to encode parasite-specific traits. Probably, a positive selection for some non-synonymous substitutions has occurred at later stages when these genes acquired new function associated with the parasitic lifestyle. The most significant gene family contractions were detected in gene families whose functions were supplemented by the host plants. Like other parasitic plants of the Orobanchaceae family, Striga evolved the ability to germinate after sensing strigolactones (SLs), which indicate the presence of a host, by co-opting a divergent subclade of KAI2 paralogs–KAI2d [3]. In S. asiatica genome, the KAI2 gene orthogroup consists of 21 members, including 17 of the KAI2d class. Most of them are highly expressed in seeds and seedlings. If different KAI2d proteins have specificity for distinct types of SLs, then the rapid evolution of the KAI2d gene subclade likely enabled Striga seeds to recognize a wide range of host plants.
In Striga hermonthica (the most devastating Striga species), twelve clusters of transcripts were defined by distinct expression profiles at different developmental stages: preconditioned seeds; seedlings 48 h after 10 nM strigol treatment; whole seedlings 1 day post infection (dpi) of rice plants; and haustoria attached to rice tissues at 3 and 7 dpi [1]. The early-stage parasitism gene expression was induced by the 2,6-dimethoxy-p-benzoquinone (DMBQ) treatments and by both host (rice) and non-host (Lotus japonicus) plant interactions, while the expression of middle- and late-stage genes was not seen in the interaction with non-host plant. Since S. hermonthica is able to penetrate into tissues of non-host plants, but not establish xylem connections with L. japonicus, these observations mean that early-stage genes are likely to be important for haustorium formation and host penetration, while the middle- and late-stage genes may be required for the xylem connection formation and the host materials acquisition. In situ hybridization analysis confirmed this view. An early-stage peroxidase was exclusively expressed in the intrusive cells at the host–parasite interface, whereas 7-dpi haustoria-specific genes were highly expressed in the hyaline body that functions as a sink for host materials. The middle- and late-stage specific genes included the hydrolase genes during host penetration, transport-related genes during host nutrient acquisition, and signal transduction-related genes during resource allocation. Specifically, enzymes targeting primary cell wall components, such as pectin, were highly up-regulated. Many protease genes were up-regulated at the later stages of infection. It has been hypothesized that parasitic plants employed a pre-existing developmental program to evolve the haustorium [4]. One such program is lateral root formation, as this also creates new xylem connections in roots. All the 18 known lateral root development (LRD) genes in A. thaliana have orthologs in the S. asiatica genome, and 17 of them were detected in the S. hermonthica transcriptome. Among these genes, SLR, ARF19, and LAX3 were specifically expressed during the early stage of haustorium development. Both SLR and ARF19 are involved in regulating the expression of LAX3 that encodes an auxin influx carrier, which localizes auxin accumulation during the LRD. Hence, the SLR-ARF19-LAX3 module may be functioning in auxin accumulation during Striga haustoria formation. Another putative target of the SLR-ARF19 is the ortholog of LATERAL ORGAN BOUNDARIES DOMAIN 18 (LBD18), which was found to be up-regulated at the early stage of haustorium development. In A. thaliana, LBD18 activates cell proliferation in the lateral root primordia. Thus, the LBD18 ortholog may function in regulating cell proliferation during haustorium formation. Interestingly, orthologs of the two LRD-related genes, ABERRANT LATERAL ROOT FORMATION 4 (ALF4) and ARABIDOPSIS CRINKLY 4 (ACR4), were not up-regulated in haustoria, but were up-regulated in the host plants at 1 dpi. It could be suggested that these genes link the interaction between Striga and its host. Taken together, these findings suggest that haustorium formation evolved, at least partly, through the recruitment by the parasitic plant of the host LRD programs.

2. Orobanche/Phelipanche

Triphysaria versicolor is a generalist parasite plant that feeds on highly diverse angiosperms, including at least 30 species in 17 families of monocot and eudicots [5]. Transcriptomes from the laser-dissected haustorium samples of T. versicolor grown on distantly related host species Zea mays and Medicago truncatula were sequenced to identify shared and host-specific patterns of gene expression. A large number of unigenes (1124) were shared between the interface transcriptomes of T. versicolor grown on both hosts, but absent from the transcriptome of above ground tissues of autotrophically grown T. versicolor. These unigenes likely represent the core set of parasite genes that are active irrespective of the host plant species. Many other unigenes were exclusive to a specific host interface (677 for Z. mays and 361 for M. truncatula), likely representing genes that interact with unique aspects of the host biology. Notably, the unigenes shared in the interaction of T. versicolor with both hosts were over-represented for the transcription factor (TF) category and under-represented for the transport category. Therefore, there are TF genes that are specifically active at the parasite–host interface but not expressed in the above ground tissues of autotrophically grown T. versicolor. In contrast, most of the transporter gene families that are expressed at the interface are also expressed in the above ground tissues. Among the most highly expressed genes in the shared interface sets were genes for β-expansin and several other cell wall modifying enzymes, a gene encoding a putative AP2-ERF domain TF, and 10 genes with sequence identity to pathogenesis-related proteins in other eudicot species. The putative β-expansin gene was highly expressed in T. versicolor interface on Z. mays, but lowly expressed in T. versicolor interface on M. truncatula. This apparently host-specific gene expression is notable because of the expansins’ role as cell-wall loosening proteins implicated in the interaction between parasitic plants and their hosts.
In another model species of Orobanchaceae family, Phtheirospermum japonicum, haustorium-inducing factors (HIFs) induce the expression of an auxin biosynthesis gene in root epidermal cells at haustorium formation sites, causing cell division and expansion to form a semispherical pre- or early haustorium structure [6]. When exposed to HIFs without a host in close proximity, haustorium formation is induced, but its growth is soon arrested. Thus, the fate of haustorium cells is determined by host availability. Two P. japonicum mutants, one dominant and one recessive, cannot regulate cell division and cell fate transitions at the haustorium apex and thus showed defects in host invasion [7]. The mutant lines had elongated haustoria on a medium containing DMBQ. Wild-type (wt) haustoria stopped growth within 2 days after DMBQ treatment, probably to suppress unnecessary growth in the absence of a host. In contrast, mutant haustoria kept elongating even after 3 days of DMBQ treatment, suggesting a defect in such a suppression system. Mutant haustoria often produce a single xylem strand, but it does not connect with root xylem. The putative mutant genes were recently identified for both of these mutants by whole genome sequencing [7]. The draft genome of P. japonicum was annotated to contain 30,337 protein encoding genes. Two non-synonymous SNPs were identified in the genome sequence of the recessive mutant, one of them located in gene encoding protein phosphatase 2C, while another in the single copy gene encoding a homolog of A. thaliana EIN2–key signal transducer of ethylene. The SNP in PjEIN2 replaces the Arg744 residue with a stop codon, resulting in truncated PjEIN2, likely defective for activating the ethylene signaling in the cell nucleus. In the dominant mutant genome sequence, 36 non-synonymous SNPs were found, of which one occurred in a gene homolog of A. thaliana ETHYLENE RESPONSE 1 (ETR1). This SNP in PjETR1 causes an Ile to Phe replacement within the first of three hydrophobic regions at the N terminus that function in ethylene binding. In A. thaliana, mutations in these hydrophobic regions result in complete loss of ETR1 ability to bind ethylene and in a dominant ethylene-insensitive phenotype. Since both mutants had SNPs in key signaling genes in the ethylene pathway, their mutant phenotypes might be caused by defects in ethylene signaling. Consistent with this assumption, both mutants were ethylene-insensitive for growth inhibition of roots and hypocotyls. Moreover, transformation of a full-length PjEIN2 sequence restored the normal haustorium phenotype in the recessive mutant. Therefore, the elongated haustorium phenotype was caused by ethylene insensitivity. Elongated haustoria were induced in wt P. japonicum by treatments with ethylene signaling inhibitors AgNO3 and 1-methylcyclopropene, mimicking the phenotype of Pjetr1 and Pjein2 mutants. AgNO3 induced elongated haustoria similarly in S. hermonthica. Ethylene biosynthesis genes and receptors are also conserved in S. asiatica [1]. Therefore, the function of ethylene signaling in haustorium elongation appears to be conserved in the Orobanchaceae. Expression of the auxin-responsive promoter DR5 coincided with haustorial apical cell proliferation, and more prolonged maxima of auxin response were observed in Pjein2 haustorium apices compared with wt. Hence, ethylene signaling may be necessary to terminate cell proliferation at the haustorium apex via suppression of the auxin response. In infection assays with A. thaliana and rice as host plants, most of the wt haustoria successfully invaded host roots, while invasion levels were significantly lower in Pjetr1 (by 65–70%) and Pjein2 (by 91–98%). Non-invaded mutant haustoria failed to develop intrusive cells at the apex and kept elongating around the host surface even after direct contact with the host roots. Thus, ethylene signaling in the parasite appears to be crucial for the haustorium apex cells to differentiate into intrusive cells for host invasion. Apparently, parasitic plants maintain haustorial apex growth until they encounter a position where the host produces ethylene.
When the P. japonicum haustoria penetrate the roots of A. thaliana, thin cell walls are observed at the site of adherence between the haustoria tips and the host plant tissue, indicating that cell wall digestion occurred at this interface [8]. Similar to the diverse host range of P. japonicum as a parasite, it has been noted to have an unusually wide range of compatible partners in interspecies grafting, both as the scion and as the stock plant. It was suggested that mechanisms of these two types of interspecies communication are somehow related. Similar to parasitic association, cross-sections of the graft junctions between P. japonicum and A. thaliana show xylem continuity and apoplastic dye transport. Therefore, P. japonicum is able to achieve tissue adhesion and vasculature connection with members of diverse plant families in both parasitism and grafting. However, the transcriptomes of the P. japonicum haustoria during A. thaliana root parasitism and those of the P. japonicum grafted regions on the A. thaliana stems were overall different. Some genes were up-regulated both during parasitism and grafting, including those associated with wound healing processes, such as auxin action, pro-cambial activity, and vascular formation. However, the expression of many other genes was distinct between parasitism and grafting. A member of the Glycosyl hydrolase 9B (GH9B) gene family, GH9B3, is known to be crucial for cell-to–cell adhesion in plant interfamily grafting. Parasitic plants P. japonicum and S. hermonthica have five and four GH9B3 genes, respectively, while only two and one such genes are present in non-parasite plants A. thaliana and Lindenbergia philippensis, respectively. This tendency for the greater number of the GH9B3 clade genes was also observed in S. asiatica. In L. philippensis, GH9B3 was up-regulated at 1 day after grafting both in compatible and incompatible interspecies grafts, but this up-regulation did not continue to increase in subsequent days. By contrast, in P. japonicum, the most highly related GH9B3 homolog was up-regulated at the early stage of both parasitism and grafting and gradually increased in subsequent days. Similar situation was observed in S. hermonthica. Some of the other homologous genes of the GH9B3 clade were also up-regulated in parasitism, but not those of the other GH9 clades. Therefore, the up-regulation of GH9B3 homologs at the sites of infection and interfamily grafting seems to be a conserved feature in parasitic plants. Amino acid sequences encoded in GH9B3 genes show a conserved catalytic domain and O-glycosylation sites. In P. japonicum, GH9B3 expression was detected at the haustorium cell periphery attaching to the host at 1–2 dpi and in the inside of haustorium at 3–4 dpi. Thus, GH9B3 appears to function at the parasite–host interface at the early adhesion stage and in xylem formation at later stages. GH9B3-knockdown by RNAi did not affect haustorium emergence but significantly reduced the number of successful xylem connections with the host. Therefore, GH9B3 positively regulates infection processes in P. japonicum. Glycosyl hydrolases encoded in the GH9B3 clade genes are probably β-1,4-glucanases that target glucan chains of cellulose in the primary cell walls. It could well be that GH9B3-down-regulated haustoria cannot reach the host vasculature due to insufficient glucanase activity to loosen the host cell wall. In P. japonicum, four of the five GH9B3 genes appear to encode fully functional proteins.
In P. japonicum and other parasitic Orobanchaceae, once the haustorium reaches host tissues, the epidermal cells of the parasite haustorium apex differentiate into intrusive cells—the specialized cells for host invasion [9]. In a recent study, differential gene expression was investigated specifically in the intrusive cells at the penetrating tips of the P. japonicum haustoria [10]. A total of 3079 differentially expressed genes (DEGs) were detected between the intrusive cells and other parts of the haustorium. Among the DEGs that showed strong and specific expression in the intrusive cells, three were the most notable. A homolog of the A. thaliana HAESA-LIKE1 (HSL1)–INTRUSIVE CELL-SPECIFIC LEUCINE-RICH REPEAT RECEPTOR-LIKE KINASE1 (ICSL1) probably functions as a peptide hormone receptor. GERMIN-LIKE PROTEIN1 (GLP1) encodes a germin-like protein closely related to the Gossypium hirsutum ABP19—a superoxide dismutase that regulates redox status. CONSTITUTIVE DISEASE RESISTANCE1 (CDR1) encodes an aspartic protease—a homolog of aspartic proteases that regulate disease resistance signaling in A. thaliana. Among the genes that were expressed at higher levels in intrusive cells than other parts of the haustorium, five genes encode subtilisin-like serine proteases (SBTs) involved in biotic interactions. Multiple SBT genes were induced in the haustorium at 3 dpi or later, indicating that these SBTs are activated after attachment to the host. Transgenic P. japonicum plants expressing the coding sequences of proteinase inhibitors Epi10 and AtSPI-1 under the control of intrusive cell-specific SBT1.1.1 and SBT1.2.3 promoters showed reduced xylem bridge formation in the haustoria at 5 days after infection of A. thaliana roots compared with control plants. Furthermore, expression of Epi10 led to decreased activity of the ICSL1 promoter in the intrusive cells and diminished auxin responses in the haustoria central region but not around the xylem plate. Collectively, these results suggest that the intrusive cell-specific SBT activities promote the auxin-dependent maturation of haustoria by regulating development of intrusive cells and subsequent xylem bridge formation. In plants, SBTs are known to function in the maturation of plant peptide hormones leading to phenotypic changes such as root elongation, abscission of floral organs, and embryonic cuticle integrity. Apparently, in parasitic plants, some SBTs might evolve for biotic interactions, including parasitism. Since many SBT clades were found to be species-specific, different parasites might recruit SBTs independently to promote parasitism.

3. Cuscuta

Unlike root parasites, the obligate parasite dodders (Cuscuta) establish haustoria on the above-ground parts of their hosts [11][12]. In an early attempt to understand the genetic makeup of dodders, the expressed genes of the two Cuscuta species, C. pentagona and C. suaveolens, were analyzed by high-throughput sequencing [13]. In sequence comparisons between Cuscuta and 12 plant species with sequenced genomes, the highest level of similarity was observed with tomato reflecting a close phylogenetic relationship of respective families (Convolvulaceae and Solanaceae) that belong to the same order (Solanales). Notably, some dodder expressed sequence tags (ESTs) showed higher similarities to transcripts of more distant plant species, such as monocots, suggesting that these dodder sequences might have been acquired via horizontal gene transfer (HGT) events. Overall, transcripts of the two dodder species showed high similarity to those of sweet potato, suggesting that few genetic features could account for their distinct lifestyles, likely through the acquisition of new functions by existing genes. Few ESTs that were highly similar between the two dodder species showed significant similarity with transcripts of other parasitic plants but had no significant sequence similarities in non-parasitic species. Obviously, the corresponding genes in the Cuscuta genomes could serve as promising targets of RNAi-based approaches to dodder resistance.
The first reference transcriptome of C. pentagona was created by de novo assembly of the massive short-read sequencing data on the Illumina HiSeq2000 platform [14]. It should be noted that the Cuscuta plants used in that study were indeed members of a closely related species Cuscuta campestris [15][16]. The resulting transcriptome encoded 44,758 putative proteins [14]. Gene expression profiles at specific stages of dodder development were not greatly influenced by the host plant species. Gene Ontology (GO) terms “cell wall” and “hydrolase activity” were enriched in the pre-haustoria-specific gene set, while “transporter activity”, “secondary metabolic process”, “response to external stimuli”, “secondary shoot formation”, and “polar auxin transport” were the most enriched terms in the haustoria-specific gene set. Multiple transcripts were up-regulated in haustoria compared with stems and seedlings. The up-regulated DEGs included genes encoding disease, defense, and drug response signals, cell wall-loosening enzymes and modulators, TFs, and auxin related proteins. Among the down-regulated DEGs were genes involved in auxin response, such as multiple INDOLE-3-ACETIC ACID INDUCIBLEs (IAAs), AUXIN RESPONSE FACTORs (ARFs), and SMALL AUXIN UPREGULATED (SAUR)-like genes.
The genes expressed in the interface region between the parasite Cuscuta japonica and the host Glycine max were studied by analyzing RNA-seq reads obtained from the interface region without physically dissecting either the parasite’s or host’s tissues [17]. Instead of physical dissection, a bioinformatic approach was used to classify the reads into either C. japonica or G. max transcriptomes. The expression profiles of all DEGs, 3819 and 17,653 of them belonging to C. japonica and G. max, respectively, were classified relative to the stages of parasitism. Multiple hydrolase enzymes appeared to be involved in molecular interactions occurring in the extracellular space at the parasite–host interface. The expression of cell wall degrading enzyme genes in C. japonica occurred at 24–48 h after attachment, when the haustoria penetration proceeded from the host cortex to the host pith, preceding the expression of expansins in G. max. The increase in the transcriptional activity of transporter genes was observed at later stage, likely reflecting the increase in sink activity of C. japonica. Simultaneous monitoring of gene expression in parasitic and host plants could assist in understanding the coordination of cellular processes between the two plants.
Gene expression in haustoria and stems of two Cuscuta species, C. reflexa and C. gronovii, was analyzed to identify the cell-wall-related genes expressed at the onset and progress of haustorium development [18]. Haustoria were induced either by infestation the compatible host plant Pelargonium zonale or in the absence of a host plant by the far-red (FR) light. Unlike the host plant infection that progressed at variable speed, the development of FR light-induced haustoria occurred at a very predictable time pace. Mostly transcripts associated with the cell wall functions were predominant among the haustorium-specific sequences, probably reflecting elevated cell wall remodeling activities in this tissue. The two XTH (xyloglucan endotransglucosylase/hydrolase) genes and the PX-2 (peroxidase) gene showed a more specific expression pattern with ≥80-fold higher expression levels in young haustoria. The xyloglucan-modifying enzymes encoded in XTH genes were shown by immunofluorescent microscopy to be located in the cell walls of elongating cells in the areas flanking the haustorial initiation center—the part that is responsible for the swelling of the stem during attachment to a host plant. Furthermore, the xyloglucan endotransglucosylation (XET) activity of XTHs was detected in the parasite throughout haustorium development, mostly at the side facing the host plant. Weaker XET activity was detected in the endophytic part of the haustorium. XTHs are known to function in loosening the plant cell walls by restructuring xyloglucans, allowing turgor-driven expansive cell growth. Seven XTH genes in C. campestris were found to be highly expressed at the pre-haustorial stage [14], suggesting that the early expression of these genes is a common developmental event in various Cuscuta species. Interestingly, the increased expression of a tomato XTH gene has been reported to be a possible defense reaction of resistant tomato interaction with C. reflexa by tightening the cell walls [19]. It well could be that the infective mechanisms in parasite plants might have evolved through re-purposing of defense pathways that already existed in their non-parasitic ancestors. The results obtained indicate that changes to cell walls are essential in the formation of the haustorium. Therefore, cell wall genes and XTH genes in particular might prove effective gene silencing targets for the control of Cuscuta in agriculture.
The first high-quality reference genomes for Cuscuta species were assembled relatively recently for C. campestris [20] and C. australis [21]. The genome sequence of C. campestris contains 44,303 predicted gene loci that were supported by transcriptome data and/or sequence similarity to known sequences [20]. Of the 1440 genes typically conserved in plants, 82.1% were present in the C. campestris assembly, and 59% of them in a duplicated form. Of the assembled sequences, 46.2% were identified as transposon-derived, mostly LTR retrotransposons. The high proportion of gene duplicates with a low synonymous substitution rate (dS) value and the recent LTR-retrotransposon proliferation pointed to a recent genome duplication event. More than thousand gene families conserved in all other tested dicots were found to lack orthologs in C. campestris. A total of 1736 genes were lost in C. campestris relative to Ipomoea nil—the closest available non-parasitic relative of Cuscuta. Most of the genes that distinguish C. campestris from non-parasitic plants appeared to be highly conserved across land plants, supporting the assumption that their function has become obsolete due to the parasitic lifestyle. In the search for putative HGT events, 64 novel candidates from at least 32 different donor sequences were found in the C. campestris genome, with a functional bias towards defense reactions or unknown functions in their hosts. Most of them could be traced back to the preferred host orders Fabales and Caryophyllales suggestive of HGT between host and parasite. Some of these transferred genes showed strong up- or down-regulation in haustorial vs. control tissues, suggesting that their gene products play a role in the infection process.
More than half of the ~273 Mbp genome sequence in C. australis appeared to consist of repetitive elements [21]. Similar to C. campestris, LTR retrotransposons are the dominant type of repeats in C. australis. Of the total 13,981 gene families that were identified in C. australis and seven reference plant species, 1256 had been significantly contracted and 478 significantly expanded in C. australis compared with phylogenetically related autotrophic plant species. Of about 12,000 conserved gene orthogroups identified in the seven reference species, 1402 were absent in C. australis. In Solanum lycopersicum and I. nil, genes of these orthogroups are preferentially expressed in leaves and roots, consistent with the absence of these organs in Cuscuta. Overall, massive loss of genes was found in gene pathways controlling leaf and root development, nutrients uptake from soil, photosynthesis, flowering time, and defense against pests and pathogens. It was found that 1124 genes underwent positive selection after the divergence between Cuscuta and their closest autotrophic relative I. nil, including those associated with hormone responses, DNA methylation, regulation of transcription, and cell wall-related metabolism. Among these genes, 115 were found to be preferentially expressed in pre-haustoria/haustoria, including genes encoding a pectin esterase, receptor-like kinases, TFs, a serine carboxypeptidase, and transport proteins. Five positively selected genes from the expanded gene families were found to be preferentially expressed in haustoria, including a gene that encodes a putative α/β-hydrolase highly similar to Nicotiana sylvestris DAD2/DWARF14 which is an SL receptor in autotrophic plants. Thus, neo-functionalization of α/β-hydrolase genes might be involved in the evolution of parasitism both in the stem parasites Cuscuta and in the root parasites Striga and Orobanche [3].
An in vitro system for inducing haustorium development outside an intact host was developed and used to examine the host-dependence of the haustoria formation in C. campestris [22]. When lateral shoot segments of C. campestris were pressed with a stack of glass slides and subjected to blue light irradiation for 72 h, two types of haustoria were induced. The haustoria with protruding search hyphae were regarded true haustoria, while the conical-shaped haustoria without searching hyphae were termed pseudohaustoria. Under these conditions, when C. campestris shoot segments did not attach to the host, elongation of axial cells and search hyphae was observed in the true haustoria, but the search hyphae did not differentiate into xylem hyphae. These true haustoria were similar to those observed just after penetration into the host stems. No visible alterations in development were observed in the true haustoria when the dodder shoot segments were exposed to the phytohormone mixtures known to induce xylem vessel differentiation in other angiosperms. Hence, the inability to induce differentiation in the absence of host tissue was not due to a lack of phytohormones derived from the host plants, but some other host-derived factors were needed to induce the xylem vessel differentiation in Cuscuta haustoria. When the lateral shoot segments of C. campestris were overlaid with fresh rosette leaves of A. thaliana, and then pressed with a stack of glass slides, haustoria invaded the host tissue and the final process in xylem vessel differentiation was observed at the contact area with the host xylem. This in vitro xylem differentiation was quite similar to that observed during C. campestris parasitization on the intact host plants. RNA-seq was used to examine the transcriptional regulation of haustorium development during the time-course of haustoria penetration into the host tissue. RNA-seq libraries were prepared from tissue samples taken at 57 h after induction (hai), when most haustoria had penetrated the host rosette leaf, and 87 hai, when differentiation of search hyphae into xylem hyphae had occurred. True haustoria that did not contact the host tissue were also used at the same time points, and epidermal and cortical cells of C. campestris at 0 hai served as a “no-haustorium” control. A total of 15,277 DEGs were identified in the haustorium compared with the “no-haustorium” sample. Of these DEGs, 4239 were shared between the four haustorium conditions. Consistent with previous gene expression studies [14][18], genes encoding functionally annotated proteins for carbohydrate metabolism, cell wall, and solute transport, as well as phytohormones, protein degradation, and RNA biosynthesis, were up-regulated in the haustorium. At 57 hai, genes encoding proteins for cell wall metabolism, phytohormones, protein modification, and secondary metabolism were significantly enriched among the DEGs up-regulated in haustoria that penetrated the host rosette leaf. At 87 hai, genes related to phytohormones, polyamine metabolism, and RNA biosynthesis were up-regulated in these haustoria. Thus, gene expression is dynamically regulated during haustoria penetration into host tissue and during their further development. When the expression of orthologous genes known to be involved in the development and proliferation of vascular stem cells, was compared at 57 hai between haustoria that penetrated the host tissue and true haustoria that were induced in the absence of the host tissue, most of these genes were up-regulated in both samples, indicating that haustoria acquired the potential for differentiation into xylem cells even in the absence of host tissue. At 87 hai, genes encoding proteins involved in the promotion of xylem vessel cell formation were not up-regulated in the haustoria that did not penetrate the host tissue. On the contrary, these genes (VND7, MYB46, MYB83, CESA4/IRX5, and CESA7/IRX3) were up-regulated in the haustoria that penetrated the host leaves in the in vitro system and in the haustoria produced by C. campestris shoots 54 h after coiling around an intact stem of A. thaliana, when search hyphae contacted the host xylem. These data show that contact of search hypha with the host xylem induces the up-regulation of a VND7 ortholog and its downstream target genes in C. campestris resulting in the formation of xylem vessel cells in the haustorium.
Though initiation and progression of haustorium in Cuscuta depend on signals from the host plant, a host-free haustorium induction by a combination of far-red (FR) light and tactile stimuli [18] or blue light [22] can be used to study the haustorium development in a more uniform and predictable experimental paradigm. A FR-induction was employed in a recent study to correlate gene expression patterns with characteristic morphological traits during successive stages of haustorium development [23]. In this experimental setup, apical portions of the C. campestris stems developed haustoria that bear many of the morphological and molecular characteristics of naturally developing haustoria. After 1–2 days, a slight bump appeared on the surface. It showed on the cross-sections that epidermal cells underwent a strong elongation perpendicular to the surface and haustorium initials appeared in the region between the cortex and the vascular tissue. This early “swelling stage” (SWE), soon became more pronounced and formed a readily visible structure of ~1–2 mm that stuck to the surface it faced—the “attaching stage” (ATT). In cross-sections at this stage, the newly formed pre-haustorium with its meristem and elongation zones was visible. The epidermal cells facing the surface were palisade-formed and dark purple stained owing to their high pectin content. Then, the haustorium emerged in the center of this lateral structure with search hyphae at its tip that sometimes protrude from the surface. In the host-free system, this was the final stage that can be observed—the “penetrating stage” (PEN), while on a host plant, the action of degrading enzymes causes a rupture in the infected tissue and the intrusion of the haustorium. Stem sections below and above the region where haustoria developed (non-infective stems or “niS”) were used as reference sites. The most profound changes in gene expression occurred during the transition between niS and SWE, with 3440 and 1500 DEGs up-regulated and down-regulated, respectively. By contrast, only about half as many DEGs were differentially regulated in the subsequent stages: 2326 in ATT relative to niS and 2554 in PEN relative to niS. In both cases, the majority of DEGs were up-regulated (1934 and 2145, respectively). Of these DEGs, 1012 were common to the three haustorial stages. The highest number of stage-specific DEGs was observed at SWE (2783), followed by PEN (943), while only 192 DEGs were specific for the transitory stage ATT. Hence, largest changes in gene expression occur in the very beginning of haustorium development. More DEGs in SWE than the two later stages support the involvement of numerous regulatory processes in the earliest step of haustoriogenesis. Among these DEGs were genes of expansins that contribute to cell wall loosening and cell expansion. Auxin-related biosynthetic enzymes and transporters, as well as 11 of the 22 alpha-class expansins were up-regulated in SWE. Other DEGs that were enriched in SWE, including those related to cell cycle, cytoskeleton and cell wall, likely coordinate meristem development and organogenesis. Beyond this initial stage, more subtle changes in gene expression may indicate that once the haustorial development has been started, relatively small adjustments are needed to advance the process further.

4. Santalaceae

Santalum album (sandalwood) is one of the economically important plant species in the Santalaceae family due to its use in the production of highly valued perfume oils. Sandalwood is also a root hemi-parasite that can produce photosynthetic products, but needs to obtain some of its water and simple nutrients from other plants through haustoria. In nature, at least 300 species, including S. album itself, can act as hosts of sandalwood tree. To identify genes and main pathways involved in haustorium development in S. album, the transcription profiles of its haustoria were studied at the pre-attachment (1 to 10 days after haustorium initiation) and post-attachment (10 to 20 days after haustorium initiation) stages [24]. Twenty-day-old non-haustorial seedling roots were collected as the control (R) sample. The majority of the S. album transcripts were expressed in all three tissue samples, indicating that very similar sets of genes underlie the haustorial and root development. Only 90, 41, and 224 transcripts were preferentially expressed in roots, pre-attachment haustoria, and post-attachment haustoria, respectively. Many genes associated with cell wall metabolism and mitochondrial respiratory chain function, were highly expressed in pre-attachment haustoria relative to roots and in post-attachment relative to pre-attachment haustoria. Most genes encoding cell wall remodeling proteins, such as pectinesterase (PE), polygalacturonase (PG) precursor, pectin lyase-like superfamily protein (PL), xyloglucan endotransglucosylase/hydrolase (XTH), and expansin-like (EXL), were up-regulated in haustoria relative to roots. Several genes encoding proteins in this functional category, such as β-D-xylosidase (XYL), pectin lyase (PL), and glycosyl hydrolase superfamily protein (GH), were further up-regulated in post-attachment relative to pre-attachment haustoria. Thus, cell wall remodeling is probably involved in the growth and differentiation of haustoria. Moreover, DEGs associated with the mitochondrial respiratory chain function were strongly up-regulated in developing haustoria, suggesting that high activity of mitochondrial respiratory function is necessary to provide energy for the rapid growth of haustoria and establishing host–parasite connections. Genes encoding ribosomal proteins were also significantly up-regulated in pre-attachment haustoria relative to roots and still more up-regulated in post-attachment haustoria. A similar up-regulation in haustoria was observed for DEGs encoding enzymes of protein turnover. These results show that ribosome biogenesis and protein turnover increase when the haustorium develops and invades the host root. The most abundant class of TFs that were differentially expressed between the haustoria and roots was GRAS. Of the GRAS TFs, 49 (96%) were up-regulated in pre-attachment haustoria relative to roots and 11 (30%) were further up-regulated in post-attachment relative to pre-attachment haustoria. Some of them were specific to haustoria, suggesting that GRAS TFs may be critical for haustorium development. A total of 191 DEGs in pairwise comparisons were associated with plant hormone biosynthesis, metabolism, and signal transduction pathways, including auxin, cytokinin (CK), gibberellin (GA), ABA, jasmonic acid (JA), ethylene (ET), and brassinosteroid (BR). The largest group (91 DEGs) was involved in auxin transport and signal transduction. The majority of auxin-related genes showed higher expression in pre-attachment haustoria relative to roots, but many of them were down-regulated in post-attachment compared with pre-attachment haustoria. Three genes of auxin influx carriers (LAX) and four genes of auxin efflux carriers (AEC) were up-regulated in pre-attachment haustoria relative to roots. All 14 DEGs encoding proteins of polar auxin transport (BIGs) were up-regulated in pre-attachment haustoria, but then down-regulated in the post-attachment haustoria, suggesting that high auxin level might be needed for the haustoria initiation.
Like S. album, Thesium chinense is a facultative root hemi-parasite belonging to the family Santalaceae. It is commonly distributed in the grasslands of Eastern Asia and, similar to S. album, can parasitize a broad range of plant species. In a recent work, the detailed transcriptomic and metabolomic changes were studied in the samples of T. chinense haustoria collected from their native habitat [25]. Haustoria initiated from fully mature roots of T. chinense invade the host root tissues with their tips. Differential expression analysis revealed 2265 DEGs between haustoria and roots of T. chinense. Of these DEGs, 801 were up-regulated and 1464 down-regulated in haustoria. Genes encoding pectin methylesterase and phenylalanine ammonia-lyase showed up-regulation in haustoria. Three auxin-related genes, SHORT INTERNODES/STYLISH (SHI/STY), PIN-LIKES7 (PILS7), and SUPPRESSOR OF G2 ALLELE SKP1 (SGT1), and two LBD genes were among the top 10 most significantly up-regulated genes in haustoria. Thus, auxin response could be one of the shared mechanisms in haustorial formation among parasitic plants. The genes related to very long chain fatty acid (VLCFA) biosynthesis, ACYL-COA OXIDASE 2 (ACX2), ACYL-COA SYNTHETASE5 (ACOS5), and ACOS7 were also up-regulated in haustoria. Besides being components of the seed storage fats, VLCFAs play a key role in regulation of cell proliferation and differentiation in plants and are involved in polar auxin transport to determine the cell polarity in lateral root development. By co-expression gene network analysis, ACOS7—the VLCFA biosynthesis gene expressed in haustoria—was shown to be a highly interconnected hub gene in a module containing several DEGs between haustoria and roots, such as the lateral root developmental genes, LBD25 and KNAT6, and another VLCFA biosynthesis gene, ACX2. Other genes related to lateral root meristem formation, SCARECROW-LIKE (SCL) and WUSCHEL-RELATED HOMEOBOX (WOX), and genes related to auxin signaling, PILS6 and AUXIN RESPONSE FACTOR 9 (ARF9), were also in this module. Collectively, these data show that strongly associated VLCFA biosynthesis genes and auxin-responsive lateral root developmental pathway genes act as a key gene network in the developmental reprogramming of T. chinense haustorial formation. Indeed, pentacosanoic acid was found to be highly abundant in haustoria probably due to the up-regulation of the VLCFA biosynthesis genes.

5. Loranthaceae

Taxillus chinensis (loranthus) is a facultative stem hemiparasite plant of Loranthaceae family that attacks other plants in multiple families. Recently transcriptome profiles of haustoria development in T. chinensis were analyzed [26]. Of the total 14,295, 15,921, and 16,402 genes that were expressed in fresh seeds, early haustoria, and adult haustoria, respectively, 12,888 genes appeared to be common, 3749 DEGs were detected between early haustoria and fresh seeds, and 4139 DEGs—between adult haustoria and fresh seeds. Among these DEGs, 1543 up-regulated and 1086 down-regulated were common to early and adult haustoria. Of the 863 TF genes that were expressed in the haustoria, 174 showed differential expression. Most of these TF DEGs were common between early and adult haustoria. Compared with seeds, 9 ethylene-responsive (ER), 5 MYB, 6 WRKY, and 11 bHLH TF genes were up-regulated in both early and late haustoria. Some TF genes were specifically up-regulated in early haustoria, including 1 ER, 4 WRKY, and 5 bHLH TF genes, while 10 ER, 5 WRKY, 6 bHLH, and 4 MYB TF genes were up-regulated in adult haustoria only. Of the total 1194 ubiquitin genes, 81 were differentially expressed in haustoria relative to fresh seeds. Among them, 17 DEGs were down-regulated in early haustoria, and 11 were also down-regulated in adult haustoria. 38 ubiquitin genes were up-regulated in early haustoria, and 26 of them were also up-regulated in adult haustoria. Notably, six ubiquitin genes were gradually up-regulated along with the haustoria development, including three polyubiquitin, two ubiquitin-40S RP, and one E3 ubiquitin-protein ligase genes. Of the 226 genes encoding disease resistance proteins (DRPs) in haustoria, 94 were differentially expressed. Of these 94 DRP DEGs, 87 were up-regulated in haustoria, of which 51 were common to early and adult haustoria; seven DRP DEGs were up-regulated and eight DRP DEGs down-regulated in adult relative to early haustoria.

6. Scrophulariaceae

Monochasma savatieri is a perennial root hemiparasite herb, which is an ingredient in traditional Chinese medicine for curing urinary and upper respiratory tract infections. In a recent study, RNA profiles in M. savatieri roots were studied before and after successful parasitism on the host plants Gardenia jasminoides [27]. The transciptomes of M. savatieri roots were compared at the two key time points—8 weeks after sowing (WAS) when the parasitic relationship with the host was still not established and 16 WAS—after establishing parasitic relationship with the host. The growth and development of M. savatieri was significantly promoted after parasitizing the host. Of the all four pairwise comparisons between these plants and the respective control M. savatieri plants that were grown in the absence of the host plants, the largest number of DEGs (46,424) were observed in 8 WAS vs 16 WAS M. savatieri parasitizing plants comparison. In parasitizing plants at 16 WAS, 27,098 DEGs were up-regulated and 19,326 DEGs down-regulated compared with 8 WAS, when the parasitic relationship with the host plant was still not established. Furthermore, in this comparison, DEGs encoding 66 TFs were identified. These TFs may have regulatory roles in the establishment of parasite–host relationship. Among these TFs, the MYB family contained the largest number of DEGs, seven putative MYBs being up-regulated upon establishment the parasite–host relationship. Interestingly, eight putative TFs of the WRKY family were down-regulated, suggesting the role of negative regulators of the establishment of parasite–host associations. In the plant hormone signal transduction pathway, the highest number of DEGs was involved in auxin signal transduction, and their expression levels were increased after establishing the parasite–host relationship. Thus, similar to other parasitic plants, the auxin pathway may play an important role in the parasite–host association.

7. Rafflesiaceae

Species in the flowering plant clade Rafflesiaceae represent the most extreme form of parasitism achieved by plants [28]. Gigantic flowers of these species emerge directly from their hosts and exhibit no obvious plant body. In its vegetative stage, the parasite resides inside the host as a thread-like filament known as the endophyte. The endophytic strand is only a single cell layer wide (uniseriate) and cells typically divide perpendicularly to its axis. It lacks any discernible cell differentiation and cytologically resembles the undifferentiated embryo. During transition to flowering, the uniseriate endophyte enters a multiseriate stage and then forms a tear-shaped mass of parasite cells lacking organ differentiation, known as the protocorm. As the protocorm grows, it begins a process of cellular differentiation. Some of the cells at the periphery differentiate into xylem that establishes the connectivity between the host and the parasite. Cells internal to the host–parasite interface at the protocorm front flatten and at later stages pull away from the rest of the protocorm to create a cushion for the floral bud as it pushes through the hard woody tissues of the host vines. The flowers mimic the putrid smell to attract the flies that pollinate them. Genetic studies in Rafflesiaceae suggested an unusual genome evolution, including the complete loss of their plastid genome and multiple HGT events. These features make Rafflesiaceae of particular interest for further comparative genomic investigation. The first genome assembly for an endophytic plant parasite has been done recently [29]. Sapria himalayana Griff. is a species of Rafflesiaceae that parasitizes three distantly related Tetrastigma species (Vitaceae) in Southeast Asia. The genome of this species appeared to have an unusually low GC content (~24%), mostly due to the high proportion (~89.6%) of the AT-rich repeat elements, while the smaller compartment consisted of the gene-rich scaffolds with higher GC content (mean 41.2%). The high number of predicted genes (~55,000) appeared to be mostly represented by a small number of abundant orthogroups consisting of transposable elements (TEs). Thus, 736 (10.9%) orthogroups that contain TE-like domains account for 35,136 (82.6%) of the validated Sapria genes. Additional gene expansion was identified in 710 (10.5%) medium-sized orthogroups (<100 gene copies each). Genes in these orthogroups are involved in various functions, including chromosome organization, DNA metabolism, and the cell cycle. Consistent with its extraordinary reduction in morphology and the life cycle, an unprecedented gene loss was found to occur during the Sapria genome evolution. Nearly half (44.4%) of the 10,880 orthogroups that are universally conserved across eudicots, are absent from the Sapria genome–more than in any other group of angiosperm parasites. Of the conserved genes lost in Sapria, 13.2% (n = 642) are also lost in Striga and Cuscuta parasitic clades. Within these convergently reduced functional categories, a far greater number of genes were lost in Sapria than in other parasites, especially of photosynthesis-related genes. The most extreme example of this tendency in Sapria is the complete loss of the plastid genome and nearly complete loss of nuclear genes that regulate plastid organization and function. Higher losses were also found in functional categories not previously seen in other parasitic plants, such as biosynthesis of ABA, protein degradation, and purine metabolism. Thus, 18 of 27 genes associated with ABA biosynthesis in A. thaliana were lost in Sapria. In the protein degradation pathway, significant gene losses occurred in the ubiquitin-proteasome-mediated protein degradation and the endopeptidase Clp-mediated protein lysis. These losses may be caused by the reduced requirement for nutrient recycling and abiotic stress response. In the purine metabolic pathway, only one homolog of nucleoside diphosphate kinase (NDPK1) and two homologs of nucleoside-triphosphatase (AYP1 and AYP2) are retained in Sapria versus four and six homologs, respectively, in A. thaliana. These reductions may reflect reduced requirements for natively produced metabolites due to their uptake from the host plant. The majority of genes in Sapria are very compact, showing fewer introns than Genlisea aurea—a carnivorous plant species that has the smallest angiosperm genome known [30]. In Sapria, at least 18.7% of the genes have lost all introns that are present in both of its closest free-living relatives, Manihot and Populus. Its highly compact genes (intron length <150 bp) are significantly enriched for housekeeping functions, such as DNA and RNA metabolism, stem cell maintenance, and reproduction. This contrasts sharply with the free-living plants whose intron size is largely independent of gene function. This feature of housekeeping genes may convey a selective advantage of more efficient transcription for parasites that rely on their host for energy and chemical resources. On the other hand, a substantial proportion of the genes in Sapria contain unusually long introns. For introns longer than 1 kb, 74% of the total length consist of TEs. A wide phylogenomic analysis of 55 plant species, including three transcriptomes from Rafflesiaceae, eighteen transcriptomes from their obligate hosts Vitaceae, and 33 published genomes spanning the angiosperm phylogeny, identified HGT events in 568 Sapria genes and pseudogenes from 81 orthogroups corresponding to 1.2% of uniquely aligned genome sequences. These HGTs range from 100 bp to 16.5 kb in length, and 62% of them are intergenic. Introns were detected in all but two HGT genes where the donor sequences contained introns, supporting previous findings that the uptake of naked foreign DNA is the primary source of HGT.

This entry is adapted from the peer-reviewed paper 10.3390/ijms24032647

References

  1. Yoshida, S.; Kim, S.; Wafula, E.K.; Tanskanen, J.; Kim, Y.M.; Honaas, L.; Yang, Z.; Spallek, T.; Conn, C.E.; Ichihashi, Y.; et al. Genome sequence of Striga asiatica provides insight into the evolution of plant parasitism. Curr. Biol. 2019, 29, 3041–3052.
  2. Yang, Z.; Wafula, E.K.; Honaas, L.A.; Zhang, H.; Das, M.; Fernandez-Aparicio, M.; Huang, K.; Bandaranayake, P.C.; Wu, B.; Der, J.P.; et al. Comparative transcriptome analyses reveal core parasitism genes and suggest gene duplication and repurposing as sources of structural novelty. Mol. Biol. Evol. 2015, 32, 767–790.
  3. Conn, C.E.; Bythell-Douglas, R.; Neumann, D.; Yoshida, S.; Whittington, B.; Westwood, J.H.; Shirasu, K.; Bond, C.S.; Dyer, K.A.; Nelson, D.C. Convergent evolution of strigolactone perception enabled host detection in parasitic plants. Science 2015, 349, 540–543.
  4. Yoshida, S.; Cui, S.; Ichihashi, Y.; Shirasu, K. The haustorium, a specialized invasive organ in parasitic plants. Annu. Rev. Plant Biol. 2016, 67, 643–667.
  5. Honaas, L.A.; Wafula, E.K.; Yang, Z.; Der, J.P.; Wickett, N.J.; Altman, N.S.; Taylor, C.G.; Yoder, J.I.; Timko, M.P.; Westwood, J.H.; et al. Functional genomics of a generalist parasitic plant: Laser microdissection of host-parasite interface reveals host-specific patterns of parasite gene expression. BMC Plant Biol. 2013, 13, 9.
  6. Ishida, J.K.; Wakatake, T.; Yoshida, S.; Takebayashi, Y.; Kasahara, H.; Wafula, E.; Depamphilis, C.W.; Namba, S.; Shirasu, K. Local auxin biosynthesis mediated by a YUCCA flavin monooxygenase regulates haustorium development in the parasitic plant Phtheirospermum japonicum. Plant Cell 2016, 28, 1795–1814.
  7. Cui, S.; Kubota, T.; Nishiyama, T.; Ishida, J.K.; Shigenobu, S.; Shibata, T.F.; Toyoda, A.; Hasebe, M.; Shirasu, K.; Yoshida, S. Ethylene signaling mediates host invasion by parasitic plants. Sci. Adv. 2020, 6, eabc2385.
  8. Kurotani, K.I.; Wakatake, T.; Ichihashi, Y.; Okayasu, K.; Sawai, Y.; Ogawa, S.; Cui, S.; Suzuki, T.; Shirasu, K.; Notaguchi, M. Host-parasite tissue adhesion by a secreted type of β-1,4-glucanase in the parasitic plant Phtheirospermum japonicum. Commun. Biol. 2020, 3, 407.
  9. Goyet, V.; Wada, S.; Cui, S.; Wakatake, T.; Shirasu, K.; Montiel, G.; Simier, P.; Yoshida, S. Haustorium inducing factors for parasitic Orobanchaceae. Front. Plant Sci. 2019, 10, 1056.
  10. Ogawa, S.; Wakatake, T.; Spallek, T.; Ishida, J.K.; Sano, R.; Kurata, T.; Demura, T.; Yoshida, S.; Ichihashi, Y.; Schaller, A.; et al. Subtilase activity in intrusive cells mediates haustorium maturation in parasitic plants. Plant Physiol. 2021, 185, 1381–1394.
  11. Fernández-Aparicio, M.; Delavault, P.; Timko, M.P. Management of infection by parasitic weeds: A review. Plants 2020, 9, 1184.
  12. Shimizu, K.; Aoki, K. Development of parasitic organs of a stem holoparasitic plant in genus Cuscuta. Front. Plant Sci. 2019, 10, 1435.
  13. Jiang, L.; Wijeratne, A.J.; Wijeratne, S.; Fraga, M.; Meulia, T.; Doohan, D.; Li, Z.; Qu, F. Profiling mRNAs of two Cuscuta species reveals possible candidate transcripts shared by parasitic plants. PLoS ONE 2013, 8, e81389.
  14. Ranjan, A.; Ichihashi, Y.; Farhi, M.; Zumstein, K.; Townsley, B.; David-Schwartz, R.; Sinha, N.R. De novo assembly and characterization of the transcriptome of the parasitic weed dodder identifies genes associated with plant parasitism. Plant Physiol. 2014, 166, 1186–1199.
  15. Costea, M.; García, M.A.; Baute, K.; Stefanović, S. Entangled evolutionary history of Cuscuta pentagona clade: A story involving hybridization and Darwin in the Galapagos. Taxon 2015, 64, 1225–1242.
  16. Shahid, S.; Kim, G.; Johnson, N.R.; Wafula, E.; Wang, F.; Coruh, C.; Bernal-Galeano, V.; Phifer, T.; Depamphilis, C.W.; Westwood, J.H.; et al. MicroRNAs from the parasitic plant Cuscuta campestris target host messenger RNAs. Nature 2018, 553, 82–85.
  17. Ikeue, D.; Schudoma, C.; Zhang, W.; Ogata, Y.; Sakamoto, T.; Kurata, T.; Furuhashi, T.; Kragler, F.; Aoki, K. A bioinformatics approach to distinguish plant parasite and host transcriptomes in interface tissue by classifying RNA-Seq reads. Plant Methods 2015, 11, 34.
  18. Olsen, S.; Striberny, B.; Hollmann, J.; Schwacke, R.; Popper, Z.; Krause, K. Getting ready for host invasion: Elevated expression and action of xyloglucan endotransglucosylases/hydrolases in developing haustoria of the holoparasitic angiosperm Cuscuta. J. Exp. Bot. 2016, 67, 695–708.
  19. Albert, M.; Werner, M.; Proksch, P.; Fry, S.C.; Kaldenhoff, R. The cell wall-modifying xyloglucan endotransglycosylase/hydrolase LeXTH1 is expressed during the defence reaction of tomato against the plant parasite Cuscuta reflexa. Plant Biol. 2004, 6, 402–407.
  20. Vogel, A.; Schwacke, R.; Denton, A.K.; Usadel, B.; Hollmann, J.; Fischer, K.; Bolger, A.; Schmidt, M.H.; Bolger, M.E.; Gundlach, H.; et al. Footprints of parasitism in the genome of the parasitic flowering plant Cuscuta campestris. Nat. Commun. 2018, 9, 2515.
  21. Sun, G.; Xu, Y.; Liu, H.; Sun, T.; Zhang, J.; Hettenhausen, C.; Shen, G.; Qi, J.; Qin, Y.; Li, J.; et al. Large-scale gene losses underlie the genome evolution of parasitic plant Cuscuta australis. Nat. Commun. 2018, 9, 2683.
  22. Kaga, Y.; Yokoyama, R.; Sano, R.; Ohtani, M.; Demura, T.; Kuroha, T.; Shinohara, N.; Nishitani, K. Interspecific signaling between the parasitic plant and the host plants regulate xylem vessel cell differentiation in haustoria of Cuscuta campestris. Front. Plant Sci. 2020, 11, 193.
  23. Bawin, T.; Bruckmüller, J.; Olsen, S.; Krause, K. A host-free transcriptome for haustoriogenesis in Cuscuta campestris: Signature gene expression identifies markers of successive development stages. Physiol. Plant. 2022, 174, e13628.
  24. Zhang, X.; Berkowitz, O.; Teixeira da Silva, J.A.; Zhang, M.; Ma, G.; Whelan, J.; Duan, J. RNA-Seq analysis identifies key genes associated with haustorial development in the root hemiparasite Santalum album. Front. Plant Sci. 2015, 6, 661.
  25. Ichihashi, Y.; Kusano, M.; Kobayashi, M.; Suetsugu, K.; Yoshida, S.; Wakatake, T.; Kumaishi, K.; Shibata, A.; Saito, K.; Shirasu, K. Transcriptomic and metabolomic reprogramming from roots to haustoria in the parasitic plant, Thesium chinense. Plant Cell Physiol. 2018, 59, 724–733.
  26. Wei, S.; Wan, L.; He, L.; Wei, Y.; Long, H.; Ji, X.; Fu, J.; Pan, L. De novo transcriptome reveals gene changes in the development of the endosperm chalazal haustorium in Taxillus chinensis (DC.) Danser. Biomed. Res. Int. 2020, 2020, 7871918.
  27. Chen, L.; Guo, Q.; Zhu, Z.; Wan, H.; Qin, Y.; Zhang, H. Integrated analyses of the transcriptome and small RNA of the hemiparasitic plant Monochasma savatieri before and after establishment of parasite-host association. BMC Plant Biol. 2021, 21, 90.
  28. Nikolov, L.A.; Davis, C.C. The big, the bad, and the beautiful: Biology of the world’s largest flowers. J. Syst. Evol. 2017, 55, 516–524.
  29. Cai, L.; Arnold, B.J.; Xi, Z.; Khost, D.E.; Patel, N.; Hartmann, C.B.; Manickam, S.; Sasirat, S.; Nikolov, L.A.; Mathews, S.; et al. Deeply altered genome architecture in the endoparasitic flowering plant Sapria himalayana Griff. (Rafflesiaceae). Curr. Biol. 2021, 31, 1002–1011.
  30. Leushkin, E.V.; Sutormin, R.A.; Nabieva, E.R.; Penin, A.A.; Kondrashov, A.S.; Logacheva, M.D. The miniature genome of a carnivorous plant Genlisea aurea contains a low number of genes and short non-coding sequences. BMC Genom. 2013, 14, 476.
More
© Text is available under the terms and conditions of the Creative Commons Attribution (CC BY) license; additional terms may apply. By using this site, you agree to the Terms and Conditions and Privacy Policy.
This entry is offline, you can click here to edit this entry!
Video Production Service
Feedback