Three-dimensional Reconstructions of Haustoria in Two Parasitic Plant Species in the Orobanchaceae

Overview

Journal Plant Physiol

Specialty Physiology

Date 2021 Apr 1

PMID 33793920

Citations 7

Authors

Natsumi Masumoto

Yuki Suzuki

Songkui Cui

Mayumi Wakazaki

Mayuko Sato

Kie Kumaishi

Arisa Shibata

Kaori M Furuta

Yasunori Ichihashi

Ken Shirasu

Kiminori Toyooka

Yoshinobu Sato

Satoko Yoshida

Affiliations

Soon will be listed here.

Abstract

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.

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References

Cui S, Wakatake T, Hashimoto K, Saucet S, Toyooka K, Yoshida S . Haustorial Hairs Are Specialized Root Hairs That Support Parasitism in the Facultative Parasitic Plant Phtheirospermum japonicum. Plant Physiol. 2015; 170(3):1492-503. PMC: 4775136. DOI: 10.1104/pp.15.01786. View

Bennett J, Mathews S . Phylogeny of the parasitic plant family Orobanchaceae inferred from phytochrome A. Am J Bot. 2011; 93(7):1039-51. DOI: 10.3732/ajb.93.7.1039. View

Peron T, Candat A, Montiel G, Veronesi C, Macherel D, Delavault P . New Insights into Phloem Unloading and Expression of Sucrose Transporters in Vegetative Sinks of the Parasitic Plant . (Pomel). Front Plant Sci. 2017; 7:2048. PMC: 5220101. DOI: 10.3389/fpls.2016.02048. View

Yang Z, Wafula E, Honaas L, Zhang H, Das M, Fernandez-Aparicio M . Comparative transcriptome analyses reveal core parasitism genes and suggest gene duplication and repurposing as sources of structural novelty. Mol Biol Evol. 2014; 32(3):767-90. PMC: 4327159. DOI: 10.1093/molbev/msu343. View

Joel D, Bar H, Mayer A, Plakhine D, Ziadne H, Westwood J . Seed ultrastructure and water absorption pathway of the root-parasitic plant Phelipanche aegyptiaca (Orobanchaceae). Ann Bot. 2011; 109(1):181-95. PMC: 3241583. DOI: 10.1093/aob/mcr261. View

Cui S, Kubota T, Nishiyama T, Ishida J, Shigenobu S, Shibata T . Ethylene signaling mediates host invasion by parasitic plants. Sci Adv. 2020; 6(44). PMC: 7608805. DOI: 10.1126/sciadv.abc2385. View

Miyashima S, Koi S, Hashimoto T, Nakajima K . Non-cell-autonomous microRNA165 acts in a dose-dependent manner to regulate multiple differentiation status in the Arabidopsis root. Development. 2011; 138(11):2303-13. DOI: 10.1242/dev.060491. View

Krupp A, Heller A, Spring O . Development of phloem connection between the parasitic plant Orobanche cumana and its host sunflower. Protoplasma. 2019; 256(5):1385-1397. DOI: 10.1007/s00709-019-01393-z. View

Liu N, Shen G, Xu Y, Liu H, Zhang J, Li S . Extensive Inter-plant Protein Transfer between Cuscuta Parasites and Their Host Plants. Mol Plant. 2019; 13(4):573-585. DOI: 10.1016/j.molp.2019.12.002. View

10.

Westwood J, Yoder J, Timko M, dePamphilis C . The evolution of parasitism in plants. Trends Plant Sci. 2010; 15(4):227-35. DOI: 10.1016/j.tplants.2010.01.004. View

11.

Spallek T, Mutuku M, Shirasu K . The genus Striga: a witch profile. Mol Plant Pathol. 2013; 14(9):861-9. PMC: 6638688. DOI: 10.1111/mpp.12058. View

12.

Mutuku J, Shirasu K . Striga. Curr Biol. 2019; 29(20):R1064-R1065. DOI: 10.1016/j.cub.2019.06.075. View

13.

Yoshida S, Kim S, Wafula E, Tanskanen J, Kim Y, Honaas L . Genome Sequence of Striga asiatica Provides Insight into the Evolution of Plant Parasitism. Curr Biol. 2019; 29(18):3041-3052.e4. DOI: 10.1016/j.cub.2019.07.086. View

14.

Ekawa M, Aoki K . Phloem-Conducting Cells in Haustoria of the Root-Parasitic Plant Phelipanche aegyptiaca Retain Nuclei and Are Not Mature Sieve Elements. Plants (Basel). 2017; 6(4). PMC: 5750636. DOI: 10.3390/plants6040060. View

15.

Wakatake T, Yoshida S, Shirasu K . Induced cell fate transitions at multiple cell layers configure haustorium development in parasitic plants. Development. 2018; 145(14). PMC: 6078332. DOI: 10.1242/dev.164848. View

16.

Ogawa S, Wakatake T, Spallek T, Ishida J, Sano R, Kurata T . Subtilase activity in intrusive cells mediates haustorium maturation in parasitic plants. Plant Physiol. 2021; 185(4):1381-1394. PMC: 8133603. DOI: 10.1093/plphys/kiaa001. View

17.

Yoshida S, Shirasu K . Multiple layers of incompatibility to the parasitic witchweed, Striga hermonthica. New Phytol. 2009; 183(1):180-189. DOI: 10.1111/j.1469-8137.2009.02840.x. View

18.

Gurney A, Slate J, Press M, Scholes J . A novel form of resistance in rice to the angiosperm parasite Striga hermonthica. New Phytol. 2006; 169(1):199-208. DOI: 10.1111/j.1469-8137.2005.01560.x. View

19.

Kokla A, Melnyk C . Developing a thief: Haustoria formation in parasitic plants. Dev Biol. 2018; 442(1):53-59. DOI: 10.1016/j.ydbio.2018.06.013. View

20.

Spallek T, Melnyk C, Wakatake T, Zhang J, Sakamoto Y, Kiba T . Interspecies hormonal control of host root morphology by parasitic plants. Proc Natl Acad Sci U S A. 2017; 114(20):5283-5288. PMC: 5441792. DOI: 10.1073/pnas.1619078114. View