Development of phloem connection between the parasitic plant Orobanche cumana and its host sunflower

Krupp, Anna; Heller, Annerose; Spring, Otmar

doi:10.1007/s00709-019-01393-z

Cited by 29 publications

(21 citation statements)

References 47 publications

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“…Similarly, immaturity of the phloem is also shown in the haustoria of root holoparasitic plant, Phelipanche aegyptiaca , which also belongs to Orobanchaceae (Ekawa and Aoki, 2017). On the other hand, formation of mature sieve elements in haustoria has been reported for Orobanche crenata and O. cumana (Dörr and Kollmann, 1995; Krupp et al, 2019). These results, together with haustorial development of Cuscuta described in this section, suggest that development of procambium-like cells and haustorial xylem vessels are observed in common, on the other hand, development of phloem is different between different parasitic plants species.…”

Section: Organogenesis Associated With Parasitic Connectionmentioning

confidence: 98%

“…Second, host factors may be involved in the differentiation of searching hypha cells into xylem and phloem conductive elements (Vaughn, 2006; Krupp et al, 2019). Upon contacting xylem vessels or phloem sieve tubes of the host, the hyphal cells of haustorium starts to differentiate into respective conductive elements, implying that hyphal cells recognize the type of host conductive elements they hit in order to differentiate into the correct elements.…”

Section: Interaction With Hostmentioning

confidence: 99%

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Development of Parasitic Organs of a Stem Holoparasitic Plant in Genus Cuscuta

Shimizu

Aoki

2019

Front. Plant Sci.

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Parasitic plants infect a broad range of plant species including economically important crops. They survive by absorbing water, minerals, and photosynthates from their hosts. To support their way of life, parasitic plants generally establish parasitic organs that allow them to attach to their hosts and to efficiently absorb substances from the vascular system of the host. Here, we summarize the recent progress in understanding the mechanisms underlying the formation of these parasitic organs, focusing on the process depicted in the stem holoparasitic genus, Cuscuta. An attachment structure called “holdfast” on the stem surface is induced by the light and contact stimuli. Concomitantly with holdfast formation, development of an intrusive structure called haustorium initiates in the inner cortex of the Cuscuta stem, and it elongates through apoplastic space of the host tissue. When haustoria reaches to host vascular tissues, they begin to form vascular conductive elements to connect vascular tissue of Cuscuta stem to those of host. Recent studies have shown parasite-host interaction in the interfacial cell wall, and regulation of development of these parasitic structures in molecular level. We also briefly summarize the role of host receptor in the control of compatibility between Cuscuta and hosts, on which occurrence of attachment structure depends, and the role of plant-to-plant transfer of long-distance signals after the establishment of conductive structure.

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Section: Organogenesis Associated With Parasitic Connectionmentioning

confidence: 98%

Section: Interaction With Hostmentioning

confidence: 99%

Development of Parasitic Organs of a Stem Holoparasitic Plant in Genus Cuscuta

Shimizu

Aoki

2019

Front. Plant Sci.

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“…Broomrape attack on previously resistant sunflower genotypes results in labelling parasite populations with the same letter, indicating the need for comparative studies of populations in different countries [36]. Better understanding of processes which condition the emergence of new virulence biotypes and their comparison is therefore needed, together with fundamental research at the cellular level of the interaction between the host and parasite in the early developmental stages [37]. The results of conducted research on virulence increase are diverse in nature.…”

Section: Current Racial Status Of Broomrape World-widementioning

confidence: 99%

Genetic and Genomic Tools in Sunflower Breeding for Broomrape Resistance

Cvejić

Radanović

Dedić

et al. 2020

Genes

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Broomrape is a root parasitic plant causing yield losses in sunflower production. Since sunflower is an important oil crop, the development of broomrape-resistant hybrids is the prime breeding objective. Using conventional plant breeding methods, breeders have identified resistant genes and developed a number of hybrids resistant to broomrape, adapted to different growing regions worldwide. However, the spread of broomrape into new countries and the development of new and more virulent races have been noted intensively. Recent advances in sunflower genomics provide additional tools for plant breeders to improve resistance and find durable solutions for broomrape spread and virulence. This review describes the structure and distribution of new, virulent physiological broomrape races, sources of resistance for introduction into susceptible cultivated sunflower, qualitative and quantitative resistance genes along with gene pyramiding and marker assisted selection (MAS) strategies applied in the process of increasing sunflower resistance. In addition, it presents an overview of underutilized biotechnological tools, such as phenotyping, -omics, and genome editing techniques, which need to be introduced in the study of sunflower resistance to broomrape in order to achieve durable resistance.

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“…A similar observation was reported in Alectra where haustorial and host phloem elements are interspaced by haustorial parenchymatic cells (Dorr et al, 1979). Based on election microscope observations and pSUC2-GFP translocation assays, which can visualize intercellular simplistic continuity between host and parasite, phloem connections are thought to occur only in holoparasitic plants (Dorr and Kollmann, 1995;Dorr, 1997;Ekawa and Aoki, 2017;Spallek et al, 2017;Krupp et al, 2019). This observation reflects the importance of phloem-mediated nutrient transfer in holoparasites whose sugar acquisition completely depends on the host.…”

Section: Discontinuity Of Sieve Elements Between a Host And A Parasitementioning

confidence: 99%

“…An obligate parasite Striga hermonthica and a facultative parasite Rhinanthus minor were reported to form oscula, tubular structures that directly penetrate host xylem vessels to form a conduit connection between the host and parasite (Dorr, 1997;Cameron et al, 2006); whereas, Orobanche crenata was reported to connect to host xylems by open pits (Dörr and Kollmann, 1976). A phloem connection has been reported in the holo (non-photosynthetic) parasitic species Orobanche crenata and cumana (Dorr and Kollmann, 1995;Krupp et al, 2019). No phloem cells were detected in the haustoria of host contact sites in hemi (photosynthetic) parasites including the obligate Striga and Alectra spp., as well as the facultative Triphysaria (Dorr et al, 1979;Ba, 1988;Heidejorgensen and Kuijt, 1993;Dorr, 1997;Kokla and Melnyk, 2018).…”

Section: Introductionmentioning

confidence: 95%

Three-dimensional reconstructions of the internal structures of haustoria in parasitic Orobanchaceae

Masumoto

Suzuki

Cui

et al. 2020

Preprint

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One-sentence summary 31Three-dimensional image reconstruction was used to visualize the spatial organization of cell types in 32 the haustoria of parasitic plants with special reference to their interaction with host roots. 33 34 Author contributions 35 SC and SY conceived the idea of this study, designed the experiment, analyzed the data and wrote the 36 manuscript. NM was responsible for color coding, FE-SEM and 3-D reconstruction. YSu and YSa 37 2 developed methods to align section images, automated the color coding process, and provided crucial 38 technical assistance for 3-D reconstruction. YI, AS and KK assisted with image handling. KT, MW and 39 MS prepared serial thin sections and performed FE-SEM. KF analyzed the AtPEAR promoter. KS 40 provided critical comments on the manuscript. 41 42 Abstract 51 Parasitic plants infect other plants by forming haustoria, specialized multicellular organs consisting of 52 several cell types each of which has unique morphological features and physiological roles associated 53 with parasitism. Understanding the spatial organization of cell types is, therefore, of great importance 54 in elucidating the functions of haustoria. Here, we report a three-dimensional (3-D) reconstruction of 55 haustoria from two Orobanchaceae species, the obligate parasite Striga hermonthica infecting rice and 56 the facultative parasite Phtheirospermum japonicum infecting Arabidopsis. Our images reveal the 57 spatial arrangements of multiple cell types inside haustoria and their interaction with host roots. The 3-58 D internal structures of haustoria highlight differences between the two parasites, particularly at the 59 xylem connection site with the host. Our study provides structural insights into how organs interact 60 between hosts and parasitic plants. 61 62 65 Approximately 4,500 species in 28 families, representing 1% of all angiosperm species, are proposed 66 to be parasitic plants (Westwood et al., 2010; Heide-Jørgensen, 2013). The common feature of parasitic 67 plants is the ability to form a specialized invasive organ called a haustorium. Unlike the unicellular 68 haustoria found in plant-infecting pathogenic fungi, haustoria in parasitic plants are multicellular organs 69 that function in host attachment, host tissue invasion and establishing a vascular connection between 70 the parasite and host for material transfer (Yoshida et al., 2016). Haustoria facilitate water and nutrient 71 acquisition as well as translocation of RNA molecules, peptides and plant hormones between the host 72 and parasite (Kim et al., 2014; Spallek et al., 2017; Shahid et al., 2018; Liu et al., 2019; Yoshida et al., 73 3 2019). Thus, haustoria act as efficient biological channels for interspecies material transfer, but the 74 internal structures and physiological functions of haustoria are largely unexplored. 75 The Orobanchaceae family contains the largest number of root parasitic species and present various 76 degrees of host dependency. An exception among Orobanchaceae family members is in the genus 77 L...

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Development of phloem connection between the parasitic plant Orobanche cumana and its host sunflower

Cited by 29 publications

References 47 publications

Development of Parasitic Organs of a Stem Holoparasitic Plant in Genus Cuscuta

Development of Parasitic Organs of a Stem Holoparasitic Plant in Genus Cuscuta

Genetic and Genomic Tools in Sunflower Breeding for Broomrape Resistance

Three-dimensional reconstructions of the internal structures of haustoria in parasitic Orobanchaceae

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