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Parasitic plants steal sugars, water, and other nutrients from host plants through a haustorial connection. Several species of parasitic plants such as witchweeds ( Striga spp.) and broomrapes ( Orobanche and Phelipanche spp.) are major biotic constraints to agricultural production. Parasitic plants are understudied compared with other major classes of plant pathogens, but the recent availability of genomic and transcriptomic data has accelerated the rate of discovery of the molecular mechanisms underpinning plant parasitism. Here, we review the current body of knowledge of how parasitic plants sense host plants, germinate, form parasitic haustorial connections, and suppress host plant immune responses. Additionally, we assess whether parasitic plants fit within the current paradigms used to understand the molecular mechanisms of microbial plant–pathogen interactions. Finally, we discuss challenges facing parasitic plant research and propose the most urgent questions that need to be answered to advance our understanding of plant parasitism. 

Abstract Host-specific interactions can maintain genetic and phenotypic diversity in parasites that attack multiple host species. Host diversity, in turn, may promote parasite diversity by selection for genetic divergence or plastic responses to host type. The parasitic weed purple witchweed [ Striga hermonthica (Delile) Benth.] causes devastating crop losses in sub-Saharan Africa and is capable of infesting a wide range of grass hosts. Despite some evidence for host adaptation and host-by- Striga genotype interactions, little is known about intraspecific Striga genomic diversity. Here we present a study of transcriptomic diversity in populations of S. hermonthica growing on different hosts (maize [ Zea mays L.] vs. grain sorghum [ Sorghum bicolor (L.) Moench]). We examined gene expression variation and differences in allelic frequency in expressed genes of aboveground tissues from populations in western Nigeria parasitizing each host. Despite low levels of host-based genome-wide differentiation, we identified a set of parasite transcripts specifically associated with each host. Parasite genes in several different functional categories implicated as important in host–parasite interactions differed in expression level and allele on different hosts, including genes involved in nutrient transport, defense and pathogenesis, and plant hormone response. Overall, we provide a set of candidate transcripts that demonstrate host-specific interactions in vegetative tissues of the emerged parasite S. hermonthica . Our study shows how signals of host-specific processes can be detected aboveground, expanding the focus of host–parasite interactions beyond the haustorial connection. 

Host–parasite coevolution can maintain high levels of genetic diversity in traits involved in species interactions. In many systems, host traits exploited by parasites are constrained by use in other functions, leading to complex selective pressures across space and time. Here, we study genome-wide variation in the staple cropSorghum bicolor(L.) Moench and its association with the parasitic weedStriga hermonthica(Delile) Benth., a major constraint to food security in Africa. We hypothesize that geographic selection mosaics across gradients of parasite occurrence maintain genetic diversity in sorghum landrace resistance. Suggesting a role in local adaptation to parasite pressure, multiple independent loss-of-function alleles at sorghumLOW GERMINATION STIMULANT 1 (LGS1)are broadly distributed among African landraces and geographically associated withS. hermonthicaoccurrence. However, low frequency of these alleles withinS. hermonthica-prone regions and their absence elsewhere implicate potential trade-offs restricting their fixation.LGS1is thought to cause resistance by changing stereochemistry of strigolactones, hormones that control plant architecture and below-ground signaling to mycorrhizae and are required to stimulate parasite germination. Consistent with trade-offs, we find signatures of balancing selection surroundingLGS1and other candidates from analysis of genome-wide associations with parasite distribution. Experiments with CRISPR–Cas9-edited sorghum further indicate that the benefit ofLGS1-mediated resistance strongly depends on parasite genotype and abiotic environment and comes at the cost of reduced photosystem gene expression. Our study demonstrates long-term maintenance of diversity in host resistance genes across smallholder agroecosystems, providing a valuable comparison to both industrial farming systems and natural communities.

 

Cowpea (Vigna unguiculata) cultivar B301 is resistant to races SG4 and SG3 of the root parasitic weedStriga 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 andin 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 controllingStrigaand other parasitic weeds thereby enhancing crop productivity and food security globally.