Smart Parasitic Nematodes Use Multifaceted Strategies to Parasitize Plants

Overview

Journal Front Plant Sci

Date 2017 Oct 20

PMID 29046680

Citations 35

Authors

Muhammad A Ali

Farrukh Azeem

Hongjie Li

Holger Bohlmann

Affiliations

Soon will be listed here.

Abstract

Nematodes are omnipresent in nature including many species which are parasitic to plants and cause enormous economic losses in various crops. During the process of parasitism, sedentary phytonematodes use their stylet to secrete effector proteins into the plant cells to induce the development of specialized feeding structures. These effectors are used by the nematodes to develop compatible interactions with plants, partly by mimicking the expression of host genes. Intensive research is going on to investigate the molecular function of these effector proteins in the plants. In this review, we have summarized which physiological and molecular changes occur when endoparasitic nematodes invade the plant roots and how they develop a successful interaction with plants using the effector proteins. We have also mentioned the host genes which are induced by the nematodes for a compatible interaction. Additionally, we discuss how nematodes modulate the reactive oxygen species (ROS) and RNA silencing pathways in addition to post-translational modifications in their own favor for successful parasitism in plants.

Citing Articles

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References

Iberkleid I, Vieira P, Engler J, Firester K, Spiegel Y, Horowitz S . Fatty acid-and retinol-binding protein, Mj-FAR-1 induces tomato host susceptibility to root-knot nematodes. PLoS One. 2013; 8(5):e64586. PMC: 3661543. DOI: 10.1371/journal.pone.0064586. View

Smant G, Stokkermans J, Yan Y, de Boer J, Baum T, Wang X . Endogenous cellulases in animals: isolation of beta-1, 4-endoglucanase genes from two species of plant-parasitic cyst nematodes. Proc Natl Acad Sci U S A. 1998; 95(9):4906-11. PMC: 20186. DOI: 10.1073/pnas.95.9.4906. View

Siddique S, Radakovic Z, De La Torre C, Chronis D, Novak O, Ramireddy E . A parasitic nematode releases cytokinin that controls cell division and orchestrates feeding site formation in host plants. Proc Natl Acad Sci U S A. 2015; 112(41):12669-74. PMC: 4611629. DOI: 10.1073/pnas.1503657112. View

Hewezi T, Juvale P, Piya S, Maier T, Rambani A, Rice J . The cyst nematode effector protein 10A07 targets and recruits host posttranslational machinery to mediate its nuclear trafficking and to promote parasitism in Arabidopsis. Plant Cell. 2015; 27(3):891-907. PMC: 4558665. DOI: 10.1105/tpc.114.135327. View

Ali M, Azeem F, Abbas A, Joyia F, Li H, Dababat A . Transgenic Strategies for Enhancement of Nematode Resistance in Plants. Front Plant Sci. 2017; 8:750. PMC: 5422515. DOI: 10.3389/fpls.2017.00750. View

Walsh E, Elmore J, Taylor C . Root-Knot Nematode Parasitism Suppresses Host RNA Silencing. Mol Plant Microbe Interact. 2017; 30(4):295-300. DOI: 10.1094/MPMI-08-16-0160-R. View

Wieczorek K, Hofmann J, Blochl A, Szakasits D, Bohlmann H, Grundler F . Arabidopsis endo-1,4-beta-glucanases are involved in the formation of root syncytia induced by Heterodera schachtii. Plant J. 2007; 53(2):336-51. DOI: 10.1111/j.1365-313X.2007.03340.x. View

Hofmann J, Szakasits D, Blochl A, Sobczak M, Daxbock-Horvath S, Golinowski W . Starch serves as carbohydrate storage in nematode-induced syncytia. Plant Physiol. 2007; 146(1):228-35. PMC: 2230564. DOI: 10.1104/pp.107.107367. View

Jaouannet M, Magliano M, Arguel M, Gourgues M, Evangelisti E, Abad P . The root-knot nematode calreticulin Mi-CRT is a key effector in plant defense suppression. Mol Plant Microbe Interact. 2012; 26(1):97-105. DOI: 10.1094/MPMI-05-12-0130-R. View

10.

Gao B, Allen R, Maier T, Davis E, Baum T, Hussey R . Identification of a New ss-1,4-endoglucanase Gene Expressed in the Esophageal Subventral Gland Cells of Heterodera glycines. J Nematol. 2009; 34(1):12-5. PMC: 2620536. View

11.

Cotton J, Lilley C, Jones L, Kikuchi T, Reid A, Thorpe P . The genome and life-stage specific transcriptomes of Globodera pallida elucidate key aspects of plant parasitism by a cyst nematode. Genome Biol. 2014; 15(3):R43. PMC: 4054857. DOI: 10.1186/gb-2014-15-3-r43. View

12.

Kikuchi T, Cotton J, Dalzell J, Hasegawa K, Kanzaki N, McVeigh P . Genomic insights into the origin of parasitism in the emerging plant pathogen Bursaphelenchus xylophilus. PLoS Pathog. 2011; 7(9):e1002219. PMC: 3164644. DOI: 10.1371/journal.ppat.1002219. View

13.

Beneventi M, da Silva Jr O, Lisei de Sa M, Pereira Firmino A, de Amorim R, Saliba Albuquerque E . Transcription profile of soybean-root-knot nematode interaction reveals a key role of phythormones in the resistance reaction. BMC Genomics. 2013; 14:322. PMC: 3701510. DOI: 10.1186/1471-2164-14-322. View

14.

Ali M, Plattner S, Radakovic Z, Wieczorek K, Elashry A, Grundler F . An Arabidopsis ATPase gene involved in nematode-induced syncytium development and abiotic stress responses. Plant J. 2013; 74(5):852-66. PMC: 3712482. DOI: 10.1111/tpj.12170. View

15.

Jones M, Payne H . Early stages of nematode-induced giant-cell formation in roots of Impatiens balsamina. J Nematol. 2009; 10(1):70-84. PMC: 2617858. View

16.

Yan Y, Smant G, Davis E . Functional screening yields a new beta-1,4-endoglucanase gene from Heterodera glycines that may be the product of recent gene duplication. Mol Plant Microbe Interact. 2001; 14(1):63-71. DOI: 10.1094/MPMI.2001.14.1.63. View

17.

Burgess T, Kelly R . Constitutive and regulated secretion of proteins. Annu Rev Cell Biol. 1987; 3:243-93. DOI: 10.1146/annurev.cb.03.110187.001331. View

18.

Robertson L, Robertson W, Sobczak M, Helder J, Tetaud E, Ariyanayagam M . Cloning, expression and functional characterisation of a peroxiredoxin from the potato cyst nematode Globodera rostochiensis. Mol Biochem Parasitol. 2000; 111(1):41-9. DOI: 10.1016/s0166-6851(00)00295-4. View

19.

Wang J, Lee C, Replogle A, Joshi S, Korkin D, Hussey R . Dual roles for the variable domain in protein trafficking and host-specific recognition of Heterodera glycines CLE effector proteins. New Phytol. 2010; 187(4):1003-1017. DOI: 10.1111/j.1469-8137.2010.03300.x. View

20.

Davis E, Hussey R, Baum T . Getting to the roots of parasitism by nematodes. Trends Parasitol. 2004; 20(3):134-41. DOI: 10.1016/j.pt.2004.01.005. View