Comparative genomics of orobanchaceous species with different parasitic lifestyles reveals the origin and stepwise evolution of plant parasitism
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Abstract Orobanchaceae is the largest family of parasitic plants, containing autotrophic and parasitic plants with all degrees of parasitism. This makes it by far the best family for studying the origin and evolution of plant parasitism. Here we provide three high-quality genomes of orobanchaceous plants, the autotrophic Lindenbergia luchunensis and the holoparasitic plants Phelipanche aegyptiaca and Orobanche cumana . Phylogenomic analysis of these three genomes together with those previously published and the transcriptomes of other orobanchaceous species, created a robust phylogenetic framework for Orobanchaceae. We found that an ancient whole-genome duplication (WGD; about 73.48 Mya), which occurred earlier than the origin of Orobanchaceae, might have contributed to the emergence of parasitism. However, no WGD events occurred in any lineage of orobanchaceous parasites except for Striga after divergence from their autotrophic common ancestor, suggesting that, in contrast to previous speculations, WGD is not associated with the emergence of holoparasitism. We detected evident convergent gene loss in all parasites within Orobanchaceae and between Orobanchaceae and dodder Cuscuta australis . The gene families in the orobanchaceous parasites showed a clear pattern of recent gains and expansions. The expanded gene families are enriched in functions related to the development of the haustorium, suggesting that recent gene family expansions may have facilitated the adaptation of orobanchaceous parasites to different hosts. This study illustrates a stepwise pattern in the evolution of parasitism in the orobanchaceous parasites, and will facilitate future studies on parasitism and the control of parasitic plants in agriculture.Keywords:
Orobanchaceae
Orobanche
Parasitic plant
Haustorium
Lineage (genetic)
Abstract Parasitic plants cause yield losses for important crops. Among these, Orobanche cumana Wallr, sunflower broomrape, is one of the major pests for sunflower. Previous studies stated that in most cases, the haustorium, a specific parasitic plant organ, penetrates host roots intercellularly. However, host cellular mechanisms involved during the parasitic cells penetration remained poorly described. We investigated sunflower root cellular behavior during haustorium penetration using various microscopy approaches including live cell imaging of inoculated transgenic fluorescent sunflower roots. We showed that the haustorium of O. cumana penetrated living sunflower root tissues, as a result of the degradation of the host cell wall and the formation of a new host trans-cellular apoplastic compartment for haustorium accommodation. Moreover, broomrape induced cell divisions in outer root tissues at very early stages of the interaction, leading to localized hypertrophy at the site of broomrape attachments. These findings are a change of paradigm in the research field of parasitic plants. They extend host root intracellular accommodation mechanisms initially shown for symbiotic and pathogenic biotrophic fungi to parasitic plants. It paves the way for future understanding and development of resistance to parasitic plants. Key message Combination of in vivo confocal, large field and transmission electron microscopy approaches revealed how intimate the relationship between the parasitic plant broomrape ( Orobanche cumana Wallr.) and its sunflower host ( Helianthus annus L.) is at very early stages of their interaction.
Haustorium
Orobanche
Helianthus annuus
Parasitic plant
Obligate parasite
Orobanchaceae
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The holoparasitic broomrape weeds (Orobanche and Phelipanche species) cause severe yield losses throughout North Africa, the Middle East, and Southern and Eastern Europe. These parasitic weeds form an haustorium at the tip of their radicles to infect the crop upon detection of the host-derived haustorium-inducing factors. Until now, the haustorial induction in the broomrapes remains less studied than in other parasitic plant species. Known haustorium-inducing factors active in hemiparasites, such as Striga and Triphysaria species, were reported to be inefficient for the induction of haustoria in broomrape radicles. In this work, the haustorium-inducing activity of p-benzoquinone and 2,6-dimethoxy-p-benzoquinone (BQ and DMBQ) on radicles of three different broomrapes, namely Orobanche cumana, Orobanche minor and Phelipanche ramosa, is reported. Additional allelopathic effects of benzoquinones on radicle growth and radicle necrosis were studied. The results of this work suggest that benzoquinones play a role in the induction of haustorium in broomrapes. Although dependent on the broomrape species assayed and the concentration of quinones used in the test, the activity of BQ appeared to be stronger than that of DMBQ. The redox property represented by p-benzoquinone, which operates in several physiological processes of plants, insects and animals, is invoked to explain this different activity. This work confirms the usefulness of benzoquinones as haustorium-inducing factors for holoparasitic plant research. The findings of this work could facilitate future studies in the infection process, such as host-plant recognition and haustorial formation.
Haustorium
Orobanche
Radicle
Orobanchaceae
Parasitic plant
Allelopathy
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Orobanche spp. (broomrapes) are holoparasites that subsist on the roots of many important crops and can considerably reduce yield. The control of Orobanche spp. includes physical, chemical and biological methods. Interactions between parasitic angiosperms and their hosts first occur at the level of parasite seed germination. The seeds of all Orobanchaceae germinate in soil under natural conditions only in response to specific chemical exudates from the host plant. This study describes the influence of different plant growth regulators and host plant root exudates on germination and development of calli from Orobanche seeds in vitro . The effect of indole‐3‐acetic acid, gibberellic acid and kinetin on the germination of Orobanche seeds varied with concentration. These plant growth regulators also affected the period of germination and the structure of calli and protrusions. An in vitro system for the collection of tobacco root exudates was established. Compounds released from the host roots of three different tobacco cultivars were found to provoke high levels of germination of the Orobanche seeds without any period of pre‐conditioning. This study developed methods for the investigation of host–parasite interactions and the effect of germination stimulants in Orobanche spp.
Orobanche
Orobanchaceae
Parasitic plant
Gibberellic acid
Kinetin
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Crop attack by parasitic weeds such as Striga and Orobanche occurs through developmental processes triggered by host chemodetection. Seeds of those weed species remain dormant in the soil until germination is triggered by host root exudates. The development of haustorium, a parasitic plant organ that invades the host to withdraw its nutrients, is also initiated in Orobanchaceae by host molecular cues. The induction of haustorium development by exogenous signals has previously been reported for Striga but not for Orobanche species. In this work, we demonstrate that sphaeropsidone and epi-sphaeropsidone, two phytotoxic cyclohexene oxides isolated from the fungus Diplodia cupressi, a causal agent of cypress canker, induce haustorium development in radicles of the parasitic weeds Striga hermonthica, Orobanche crenata, and Orobanche cumana. This is the first report of chemical stimulation of haustorium development in radicles of Orobanche in the absence of host. In addition, SAR studies were carried out by testing the haustorium-inducing activity of the natural cyclohexene oxides, seven already known and four new hemisynthetic derivatives, in O. cumana, O. crenata, and S. hermonthica, to find a molecular specificity model required for haustorium induction. The results suggested that the haustorium-inducing activity is due to the possibility to convert the natural sphaeropsidone and natural and hemisynthetic derivatives in the corresponding 3-methoxyquinone and that the stereochemistry at C-5 also seems to affect this activity.
Haustorium
Orobanche
Parasitic plant
Orobanchaceae
Striga hermonthica
Radicle
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Abstract Orobanchaceae parasitic plants are major threats to global food security, causing severe agricultural damage worldwide. Parasitic plants derive water and nutrients from their host plants through multicellular organs called haustoria. The formation of a prehaustorium, a primitive haustorial structure, is provoked by host-derived haustorium-inducing factors (HIFs). Quinones, including 2,6-dimethoxy- p -benzoquinone (DMBQ), and phenolics, including syringic acid, are of most potent HIFs for various species in Orobanchaceae, but except non-photosynthetic holoparasites, Phelipanche and Orobanche spp. On the other hand, cytokinin phytohormones was reported to induce prehaustoria in Phelipanche ramosa . However, little is known about whether cytokinins act as HIFs in the other parasitic species. Moreover, the signaling pathways for quinones, phenolics and cytokinins in prehaustorium induction are not well understood. This study showed that cytokinins act as HIFs in Striga hermonthica but not in Phtheirospermum japonicum . Using chemical inhibitors for each type of HIF, we demonstrated that cytokinins activate prehaustorium formation through a signaling pathway that overlaps with the quinone and phenolic HIF pathways in S. hermonthica . Host root exudates activated S. hermonthica cytokinin biosynthesis and signaling genes, and inhibitors blocking any of three types of HIFs perturbed the prehaustorium-inducing activity of exudates, indicating that host root exudates include a mixture of HIFs. Our study reveals the importance of cytokinins for prehaustorium formation in obligate parasitic plants.
Striga hermonthica
Haustorium
Orobanche
Parasitic plant
Orobanchaceae
Strigolactone
Obligate parasite
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Summary Parasitic plants of the Orobanchaceae are known as obligate root parasites that develop haustoria that connect to roots of various host plants. This article describes, for the first time, a case where the root parasite successfully connected to potato tubers, i.e. to the swollen portion of an underground stem rather than to a root. The rhizosphere of Orobanche aegyptiaca and of its host Solanum tuberosum (potato) was carefully examined. In anatomical studies, the adventitious roots were directly connected to potato tubers. Numerous secondary haustoria, which developed along the adventitious roots in close vicinity to the potato tuber, penetrated the tuber epidermis and the perimedullary tuber parenchyma and developed xylem strands that are presumably connected to the minor xylem strands within the tuber cortex. These findings indicate that parasites of the Orobanchaceae that normally attack host roots may also parasitise underground stem tubers.
Haustorium
Orobanche
Orobanchaceae
Parasitic plant
Parenchyma
Obligate parasite
Solanum tuberosum
Fibrous root system
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Orobanche and Cuscuta are two completely different types of holoparasitic plants that behave as devastating weeds on many economically important crops and pose serious challenges in their management. They are phaneroamic and non-photosynthetic plants which require other host plants for their nutrient requirement. In the present study both Orobanche and Cuscuta were compared in terms of their morphology, anatomy and pathology. The study helps in understanding the differences in the target site of the parasites, viz. leaf and stem for Cuscuta and roots for Orobanche and the difference in their ecology. The seeds of the two parasitic weeds showed morphological differences, viz. in their seed size, coat structure and texture. The conditions for germination of Orobanche was very stringent and followed certain defined sequence in terms of water absorption, pre-conditioning, sensitivity to germination stimulants. However, the germination of Cuscuta was more spontaneous and moisture was the major requirement. Post-germination development of both the parasitic weeds was result of the chemotropic response of the receptors in the parasites tothe stimuli from the host. Cuscuta and Orobanche represent different lineages of evolution in their parasitic nature and have different haustorial anatomy. Parasitization of the host was very rapid in Cuscuta (27-31 days) with multiple haustorial connections with the host stem, leaf, petiole, fruits and even on its own stem when compared to Orobanche with mostly single point of entry into the host and about 45-60 days to emerge above ground to produce a floral stalk.
Cuscuta
Orobanche
Haustorium
Parasitic plant
Orobanchaceae
Obligate parasite
Seed predation
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Root parasites of the genus Orobanche are serious weeds in agriculture. An aseptic infection system of host roots using calli of three Orobanche species was developed for the study of host-parasite interaction. The response of calli to various hormonal combinations was studied, because a requirement for infection is the differentiation of root-like protrusions, which are capable of producing haustorial connections to the host. Infectious root-like protrusions develop under the influence of 0.5-1.0 mg l(-1) IAA, and under the combination of 0.2 mg l(-1) NAA with 5.0 mg l(-1) kinetin. These protocols produced root protrusions with pad-like structures that resembled attachment organs of Orobanche seedlings, and proved effective in parasitizing host roots. Direct contact with the medium inhibited haustorium development and prevented infection. To overcome this problem, certain root portions were isolated from the medium by inserting thin glass plates underneath. Calli were then placed on the raised root portions and successfully infected the roots and developed young Orobanche tubercles with vascular system that directly connected to the host.
Haustorium
Orobanche
Parasitic plant
Orobanchaceae
Kinetin
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Citations (74)
Orobanchaceae parasitic plants are major threats to global food security, causing severe agricultural damage worldwide. Parasitic plants derive water and nutrients from their host plants through multicellular organs called haustoria. The formation of a prehaustorium, a primitive haustorial structure, is provoked by host-derived haustorium-inducing factors (HIFs). Quinones, including 2,6-dimethoxy-p-benzoquinone (DMBQ), are of the most potent HIFs for various species in Orobanchaceae, but except non-photosynthetic holoparasites, Phelipanche and Orobanche spp. Instead, cytokinin (CK) phytohormones were reported to induce prehaustoria in Phelipanche ramosa. However, little is known about whether CKs act as HIFs in the other parasitic species to date. Moreover, the signaling pathways for quinones and CKs in prehaustorium induction are not well understood. This study shows that CKs act as HIFs in the obligate parasite Striga hermonthica but not in the facultative parasite Phtheirospermum japonicum. Using chemical inhibitors and marker gene expression analysis, we demonstrate that CKs activate prehaustorium formation through a CK-specific signaling pathway that overlaps with the quinone HIF pathway at downstream in S. hermonthica. Moreover, host root exudates activated S. hermonthica CK biosynthesis and signaling genes, and DMBQ and CK inhibitors perturbed the prehaustorium-inducing activity of exudates, indicating that host root exudates include CKs. Our study reveals the importance of CKs for prehaustorium formation in obligate parasitic plants.
Haustorium
Striga hermonthica
Orobanche
Parasitic plant
Obligate parasite
Orobanchaceae
Obligate
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Haustorium
Parasitic plant
Orobanchaceae
Obligate parasite
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Citations (25)