Adaptation of the parasitic plant lifecycle: germination is controlled by essential host signaling molecules

Parasitic plants are plants that connect with a haustorium to the vasculature of another, host, plant from which they absorb water, assimilates, and nutrients. Because of this parasitic lifestyle, parasitic plants need to coordinate their lifecycle with that of their host. Parasitic plants have evolved a number of host detection/host response mechanisms of which the germination in response to chemical host signals in one of the major families of parasitic plants, the Orobanchaceae, is a striking example. In this update review, we discuss these germination stimulants. We review the different compound classes that function as germination stimulants, how they are produced, and in which host plants. We discuss why they are reliable signals, how parasitic plants have evolved mechanisms that detect and respond to them, and whether they play a role in host specificity. The advances in the knowledge underlying this signaling relationship between host and parasitic plant have greatly improved our understanding of the evolution of plant parasitism and are facilitating the development of more effective control measures in cases where these parasitic plants have developed into weeds.

Root parasitic plants grow on the roots of other plants and germinate only in the presence of that host, on which they completely depend, through the perception of host presence signaling molecules called germination stimulants.

Outstanding questions

• Have we overlooked the role of germination stimulants in facultative parasites?
• What is the biological relevance of the observation that many plant species produce and secrete a range of different strigolactones?
• Have parasitic plants evolved mechanisms to compensate for low phosphorus availability, a condition that stimulates their germination?
• What is the contribution of the HTL strigolactone receptors to host specificity in parasitic plants or does downstream signaling play a role?
• What other, nonstrigolactone, germination stimulants can parasitic plants respond to and does this require adaptation in the HTL receptors?
• What is the role of germination and underlying mechanism in the rapid adaptation of (orobanchaceous) parasitic plants to a new host?

     

Three-dimensional reconstructions of haustoria in two parasitic plant species in the Orobanchaceae

Parasitic plants infect other plants by forming haustoria, specialized multicellular organs consisting of several cell types, each of which has unique morphological features and physiological roles associated with parasitism. Understanding the spatial organization of cell types is, therefore, of great importance in elucidating the functions of haustoria. Here, we report a three-dimensional (3-D) reconstruction of haustoria from two Orobanchaceae species, the obligate parasite Striga hermonthica infecting rice (Oryza sativa) and the facultative parasite Phtheirospermum japonicum infecting Arabidopsis (Arabidopsis thaliana). In addition, field-emission scanning electron microscopy observation revealed the presence of various cell types in haustoria. Our images reveal the spatial arrangements of multiple cell types inside haustoria and their interaction with host roots. The 3-D internal structures of haustoria highlight differences between the two parasites, particularly at the xylem connection site with the host. Our study provides cellular and structural insights into haustoria of S. hermonthica and P. japonicum and lays the foundation for understanding haustorium function.

Three-dimensional image reconstruction visualized the spatial organization of cell types in the haustoria of the Orobanchaceae parasitic plants Striga hermonthica and Phtheirospermum japonicum.     

Mechanisms of resistance and virulence in parasitic plant–host interactions

Parasitic plants pose a major biotic threat to plant growth and development and lead to losses in crop productivity of billions of USD annually. By comparison with “normal” autotrophic plants, parasitic plants live a heterotrophic lifestyle and rely on water, solutes and to a greater (holoparasitic plants) or lesser extent (hemiparasitic plants) on sugars from other host plants. Most hosts are unable to detect an infestation by plant parasites or unable to fend off these parasitic invaders. However, a few hosts have evolved defense strategies to avoid infestation or protect themselves actively post-attack often leading to full or partial resistance. Here, we review the current state of our understanding of the defense strategies to plant parasitism used by host plants with emphasis on the active molecular resistance mechanisms. Furthermore, we outline the perspectives and the potential of future studies that will be indispensable to develop and breed resistant crops.

Some plants are able to recognize parasitic plants as attacking pathogens and can fend them off by inducing defense responses.

Advances

• Receptor proteins have been discovered in host plants (i.e. sunflower, tomato, or cowpea) that detect parasitic plants as an invading pathogen and further induce plant immunity and resistance responses in hosts leading to a parasite rejection.
• Molecular patterns exist in parasitic plants that can be specifically detected by host plant receptors.
• The host plant receptors require co-receptors and signaling components (i.e. BAK1, SOBIR1, etc.) also known from plant immunity against microbes.
• Parasitic plants evolved strategies to circumvent and to suppress host plant immunity, i.e. by manipulating host cells with siRNAs or proteins that act as effectors.
• Similar to the interaction of plants with microbial pathogens, elements of PTI and ETI can be both observed in plant–parasitic plant interactions.

     

Hormonal impact on photosynthesis and photoprotection in plants

Photosynthesis is not only essential for plants, but it also sustains life on Earth. Phytohormones play crucial roles in developmental processes, from organ initiation to senescence, due to their role as growth and developmental regulators, as well as their central role in the regulation of photosynthesis. Furthermore, phytohormones play a major role in photoprotection of the photosynthetic apparatus under stress conditions. Here, in addition to discussing our current knowledge on the role of the phytohormones auxin, cytokinins, gibberellins, and strigolactones in promoting photosynthesis, we will also highlight the role of abscisic acid beyond stomatal closure in modulating photosynthesis and photoprotection under various stress conditions through crosstalk with ethylene, salicylates, jasmonates, and brassinosteroids. Furthermore, the role of phytohormones in controlling the production and scavenging of photosynthesis-derived reactive oxygen species, the duration and extent of photo-oxidative stress and redox signaling under stress conditions will be discussed in detail. Hormones have a significant impact on the regulation of photosynthetic processes in plants under both optimal and stress conditions, with hormonal interactions, complementation, and crosstalk being important in the spatiotemporal and integrative regulation of photosynthetic processes during organ development at the whole-plant level.

In addition to mediating stoma-induced reductions in photosynthesis during stress, phytohormones modulate the spatiotemporal and integrative regulation of photosynthetic and photoprotection processes.

Advances

• Hormones strongly impact photosynthesis, both indirectly and directly.
• Not only CKs, but also auxin, GAs, and SLs are essential to modulate photosynthetic rates under optimal conditions at the whole-plant level.
• ABA, JAs, SA, and ethylene play a major role in the regulation of photosynthesis under various stress conditions.
• An integrated hormonal response at the whole-plant level allows the most adequate photosynthetic response to every developmental and stress situation.

     

WARPP—web application for the research of parasitic plants

The lifestyle of parasitic plants is associated with peculiar morphological, genetic, and physiological adaptations that existing online plant-specific resources fail to adequately represent. Here, we introduce the Web Application for the Research of Parasitic Plants (WARPP) as an online resource dedicated to advancing research and development of parasitic plant biology. WARPP is a framework to facilitate international efforts by providing a central hub of curated evolutionary, ecological, and genetic data. The first version of WARPP provides a community hub for researchers to test this web application, for which curated data revolving around the economically important Broomrape family (Orobanchaceae) is readily accessible. The initial set of WARPP online tools includes a genome browser that centralizes genomic information for sequenced parasitic plant genomes, an orthogroup summary detailing the presence and absence of orthologous genes in parasites compared with nonparasitic plants, and an ancestral trait explorer showing the evolution of life-history preferences along phylogenies. WARPP represents a project under active development and relies on the scientific community to populate the web app’s database and further the development of new analysis tools. The first version of WARPP can be securely accessed at https://parasiticplants.app. The source code is licensed under GNU GPLv2 and is available at https://github.com/wickeLab/WARPP.

The WARPP online resource is a new, expandable, and interactive parasitic plant-specific data hub that provides online tools tailored to the peculiarities of parasitic angiosperms.     

Subtilase activity in intrusive cells mediates haustorium maturation in parasitic plants

Parasitic plants that infect crops are devastating to agriculture throughout the world. These parasites develop a unique inducible organ called the haustorium that connects the vascular systems of the parasite and host to establish a flow of water and nutrients. Upon contact with the host, the haustorial epidermal cells at the interface with the host differentiate into specific cells called intrusive cells that grow endophytically toward the host vasculature. Following this, some of the intrusive cells re-differentiate to form a xylem bridge (XB) that connects the vasculatures of the parasite and host. Despite the prominent role of intrusive cells in host infection, the molecular mechanisms mediating parasitism in the intrusive cells remain poorly understood. In this study, we investigated differential gene expression in the intrusive cells of the facultative parasite Phtheirospermum japonicum in the family Orobanchaceae by RNA-sequencing of laser-microdissected haustoria. We then used promoter analyses to identify genes that are specifically induced in intrusive cells, and promoter fusions with genes encoding fluorescent proteins to develop intrusive cell-specific markers. Four of the identified intrusive cell-specific genes encode subtilisin-like serine proteases (SBTs), whose biological functions in parasitic plants are unknown. Expression of SBT inhibitors in intrusive cells inhibited both intrusive cell and XB development and reduced auxin response levels adjacent to the area of XB development. Therefore, we propose that subtilase activity plays an important role in haustorium development in P. japonicum.

Subtilases specifically expressed in intrusive cells regulate auxin-mediated host–parasite connections in the parasitic plant Phtheirospermum japonicum.     

Live monitoring of plant redox and energy physiology with genetically encoded biosensors

Genetically encoded biosensors pave the way for understanding plant redox dynamics and energy metabolism on cellular and subcellular levels.

ADVANCES

• Methodological advances in fluorescent protein-based in vivo biosensing have been instrumental for several paradigm shifts in our understanding of cell physiology, metabolism and signaling.
• An increasing number of genetically encoded biosensors has been used to dissect the dynamics of several distinct redox couples and energy physiology in plants.
• In vivo monitoring using biosensors has pioneered the simultaneous read-out of different physiological parameters in different subcellular locations by parallelized plate reader-based, multiwell fluorimetry, or expression strategies for multiple sensors in parallel.
• Sensing dynamic changes in hydrogen peroxide levels is possible with sensors of the HyPer family, or roGFP fusion variants with a thiol peroxidase.
• Peredox and SoNar family sensors enable direct visualization of NADH/NAD⁺, while iNAP family sensors respond to NADPH concentration in plants.
• Sensor variants with different sensitivity ranges enable use of the most appropriate variant for the specific in vivo environment or experimental scope.

     

The bright side of parasitic plants: what are they good for?

Parasitic plants are mostly viewed as pests. This is caused by several species causing serious damage to agriculture and forestry. There is however much more to parasitic plants than presumed weeds. Many parasitic plans exert even positive effects on natural ecosystems and human society, which we review in this paper. Plant parasitism generally reduces the growth and fitness of the hosts. The network created by a parasitic plant attached to multiple host plant individuals may however trigger transferring systemic signals among these. Parasitic plants have repeatedly been documented to play the role of keystone species in the ecosystems. Harmful effects on community dominants, including invasive species, may facilitate species coexistence and thus increase biodiversity. Many parasitic plants enhance nutrient cycling and provide resources to other organisms like herbivores or pollinators, which contributes to facilitation cascades in the ecosystems. There is also a long tradition of human use of parasitic plants for medicinal and cultural purposes worldwide. Few species provide edible fruits. Several parasitic plants are even cultivated by agriculture/forestry for efficient harvesting of their products. Horticultural use of some parasitic plant species has also been considered. While providing multiple benefits, parasitic plants should always be used with care. In particular, parasitic plant species should not be cultivated outside their native geographical range to avoid the risk of their uncontrolled spread and the resulting damage to ecosystems.

Advances

• Parasitic plants may act as highways for transferring systemic signals among host plants.
• Harmful effects of parasitic plants on individual hosts suppress community dominants including invasive species, reduce competitive pressure, and may increase biodiversity.
• Parasitic plants enhance nutrient cycling and provide resources for other organisms thus contributing to facilitation cascades in ecosystems.
• Many parasitic plants are recorded to have medicinal values against a broad range of diseases.
• There is a long tradition of worldwide human use of parasitic plants, which have been cultivated for their products and aesthetic values.

     

Smoke signals and seed dormancy: Where next for MAX2?

The Arabidopsis thaliana F-box protein MAX2 has been discovered in four separate genetic screens, indicating that it has roles in leaf senescence, seedling photosensitivity, shoot outgrowth and seed germination. Both strigolactones and karrikins can regulate A. thaliana seed germination and seedling photomorphogenesis in a MAX2-dependent manner, but only strigolactones inhibit shoot branching. How MAX2 mediates specific responses to both classes of structurally-related signals, and the origin of its dual role remains unknown. The moss Physcomitrella patens utilizes strigolactones and MAX2 orthologs are present across the land plants, suggesting that this signaling system could have an ancient origin. The seed of parasitic Orobanchaceae species germinate preferentially in response to strigolactones over karrikins, and putative Orobanchaceae MAX2 orthologs form a sub-clade distinct from those of other dicots. These observations suggest that lineage-specific evolution of MAX2 may have given rise to specialized responses to these signaling molecules.Key words: karrikins, strigolactones, F-box protein, seed germination, photomorphogenesis, parasitic weeds, mycorrhiza, moss, axillary branching     

The Physcomitrium (Physcomitrella) patens PpKAI2L receptors for strigolactones and related compounds function via MAX2-dependent and -independent pathways

In angiosperms, the α/β hydrolase DWARF14 (D14), along with the F-box protein MORE AXILLARY GROWTH2 (MAX2), perceives strigolactones (SL) to regulate developmental processes. The key SL biosynthetic enzyme CAROTENOID CLEAVAGE DIOXYGENASE8 (CCD8) is present in the moss Physcomitrium patens, and PpCCD8-derived compounds regulate moss extension. The PpMAX2 homolog is not involved in the SL response, but 13 PpKAI2LIKE (PpKAI2L) genes homologous to the D14 ancestral paralog KARRIKIN INSENSITIVE2 (KAI2) encode candidate SL receptors. In Arabidopsis thaliana, AtKAI2 perceives karrikins and the elusive endogenous KAI2-Ligand (KL). Here, germination assays of the parasitic plant Phelipanche ramosa suggested that PpCCD8-derived compounds are likely noncanonical SLs. (+)-GR24 SL analog is a good mimic for PpCCD8-derived compounds in P. patens, while the effects of its enantiomer (−)-GR24, a KL mimic in angiosperms, are minimal. Interaction and binding assays of seven PpKAI2L proteins pointed to the stereoselectivity toward (−)-GR24 for a single clade of PpKAI2L (eu-KAI2). Enzyme assays highlighted the peculiar behavior of PpKAI2L-H. Phenotypic characterization of Ppkai2l mutants showed that eu-KAI2 genes are not involved in the perception of PpCCD8-derived compounds but act in a PpMAX2-dependent pathway. In contrast, mutations in PpKAI2L-G, and -J genes abolished the response to the (+)-GR24 enantiomer, suggesting that PpKAI2L-G, and -J proteins are receptors for moss SLs.

The study of moss PpKAI2L receptors for strigolactones and related compounds highlights MORE AXILLARY GROWTH2-dependent and -independent pathways for the perception of these compounds.     

Strigolactones: new plant hormones in action

Main conclusion

The key step in the mode of action of strigolactones is the enzymatic detachment of the D-ring. The thus formed hydroxy butenolide induces conformational changes of the receptor pocket which trigger a cascade of reactions in the signal transduction.

Abstract

Strigolactones (SLs) constitute a new class of plant hormones which are of increasing importance in plant science. For the last 60 years, they have been known as germination stimulants for parasitic plants. Recently, several new bio-properties of SLs have been discovered such as the branching factor for arbuscular mycorrhizal fungi, regulation of plant architecture (inhibition of bud outgrowth and of shoot branching) and the response to abiotic factors, etc. To broaden horizons and encourage new ideas for identifying and synthesising new and structurally simple SLs, this review is focused on molecular aspects of this new class of plant hormones. Special attention has been given to structural features, the mode of action of these phytohormones in various biological actions, the design of SL analogs and their applications.

     

Holoparasitic plant–host interactions and their impact on Mediterranean ecosystems

Although photosynthesis is essential to sustain life on Earth, not all plants use sunlight to synthesize nutrients from carbon dioxide and water. Holoparasitic plants, which are important in agricultural and natural ecosystems, are dependent on other plants for nutrients. Phytohormones are crucial in holoparasitic plant–host interactions, from seed germination to senescence, not only because they act as growth and developmental regulators, but also because of their central role in the regulation of host photosynthesis and source–sink relations between the host and the holoparasitic plant. Here, we compile and discuss current knowledge on the impact and ecophysiology of holoparasitic plants (such as the broomrapes Orobanche sp. and Phelipanche sp.) that infest economically important dicotyledonous crops in Mediterranean agroecosystems (legumes [Fabaceae], sunflowers [Helianthus sp.], or tomato [Solanum lycopersicum] plants). We also highlight the role of holoparasitic plant–host interactions (such as those between Cytinus hypocistis and various shrubs of the genus Cistus) in shaping natural Mediterranean ecosystems. The roles of phytohormones in controlling plant–host interactions, abiotic factors in parasitism, and the biological significance of natural seed banks and how dormancy and germination are regulated, will all be discussed. Holoparasitic plants are unique organisms; improving our understanding of their interaction with hosts as study models will help us to better manage parasitic plants, both in agricultural and natural ecosystems.

Advances

• Mediterranean ecosystems represent unique environments to study holoparasitic plant-host interactions
• Holoparasitic plants cause severe reductions in productivity, but can also exert positive effects on diversity in natural ecosystems
• A bidirectional flux of phytohormones occurs in holoparasitic plant-host interactions
• The establishment of seed banks is essential for the success of both Orobanche and Cytinus infection in Mediterranean ecosystems

     

Motif-based endomembrane trafficking

Endomembrane trafficking, which allows proteins and lipids to flow between the different endomembrane compartments, largely occurs by vesicle-mediated transport. Transmembrane proteins intended for transport are concentrated into a vesicle or carrier by undulation of a donor membrane. This is followed by vesicle scission, uncoating, and finally, fusion at the target membrane. Three major trafficking pathways operate inside eukaryotic cells: anterograde, retrograde, and endocytic. Each pathway involves a unique set of machinery and coat proteins that pack the transmembrane proteins, along with their associated lipids, into specific carriers. Adaptor and coatomer complexes are major facilitators that function in anterograde transport and in endocytosis. These complexes recognize the transmembrane cargoes destined for transport and recruit the coat proteins that help form the carriers. These complexes use either linear motifs or posttranslational modifications to recognize the cargoes, which are then packaged and delivered along the trafficking pathways. In this review, we focus on the different trafficking complexes that share a common evolutionary branch in Arabidopsis (Arabidopsis thaliana), and we discuss up-to-date knowledge about the cargo recognition motifs they use.

Trafficking protein complexes recognize specific linear motifs or modifications on integral membrane proteins and this recognition guides their transport between the different cellular compartments.

ADVANCED

• Plant research is slowly gaining insight into the linear trafficking motifs used by the various AP complexes.Recent observations point out that steady-state accumulation of cargo proteins at the plasma membrane is not necessarily caused by to impaired internalization.
• TSET/TPC, the most recently identified member of the heterotetrameric adaptor complex-containing coat (HTAC-CC) family, and the identification of an endocytic-autophagosomal degradation pathway operating between the contact sites of the endoplasmic reticulum with the plasma membrane and the vacuole provide previously undiscovered additional layers of complexity to endomembrane trafficking in plants.

     

Contemporary proteomic strategies for cysteine redoxome profiling

Protein cysteine residues are susceptible to oxidative modifications that can affect protein functions. Proteomic techniques that comprehensively profile the cysteine redoxome, the repertoire of oxidized cysteine residues, are pivotal towards a better understanding of the protein redox signaling. Recent technical advances in chemical tools and redox proteomic strategies have greatly improved selectivity, in vivo applicability, and quantification of the cysteine redoxome. Despite this substantial progress, still many challenges remain. Here, we provide an update on the recent advances in proteomic strategies for cysteine redoxome profiling, compare the advantages and disadvantages of current methods and discuss the outstanding challenges and future perspectives for plant redoxome research.

Current cysteine redoxome profiling can characterize systematically diverse oxidative posttranslational modifications

Advances

• The chemical toolbox for Cys redoxome profiling has extensively expanded.
• Advanced chemoproteomic platforms have been applied to target specific Cys oxidative posttranslational modifications (OxiPTMs).
• Various reductomic workflows have been widely implemented for reversible Cys OxiPTMs quantification.
• Workflows have been integrated to measure the occupancy of multiple OxiPTMs simultaneously.
• Disulfide-based traps enable the in situ profiling for –SOH sites.

     

Current progress in Striga management

The Striga, particularly S. he rmonthica, problem has become a major threat to food security, exacerbating hunger and poverty in many African countries. A number of Striga control strategies have been proposed and tested during the past decade, however, further research efforts are still needed to provide sustainable and effective solutions to the Striga problem. In this paper, we provide an update on the recent progress and the approaches used in Striga management, and highlight emerging opportunities for developing new technologies to control this enigmatic parasite.

Advances

• The recently established Striga control technologies, such as push-pull, toothpick, and imidazolinone seed dressing have opened up new opportunities for smallholder farmers to overcome this parasite.
• The development of low-cost and efficient germination stimulants together with an application protocol for rain-fed agriculture has made the suicidal germination strategy a realistic approach.
• Molecular elucidation of strigolactone biosynthesis and perception has led to the development of new chemicals that disrupt the communication between Striga and its hosts.