Elsevier

Advances in Botanical Research

Volume 73, March 2015, Pages 189-219
Advances in Botanical Research

Chapter Eight - Recent Advances in Understanding Plant–Nematode Interactions in Monocots

https://doi.org/10.1016/bs.abr.2014.12.006Get rights and content

Abstract

Monocotyledonous crops including cereals, sugar cane, banana and cassava make an important tribute to agricultural commodities both in production and value worldwide. Diseases caused by nematodes in monocots are well documented and new data are emerging on interactions of these pathogens with some important monocotyledonous crop species. This review focuses on major monocotyledonous plant–nematode systems describing the biology and genetics of some interactions and highlighting efforts to identify and select resistant genetic resources. Molecular and histological data are presented having in the spotlight sedentary nematodes of the suborder Tylenchina. Histological observations are presented during nematode development and host resistance responses, comparing monocot and dicot plant hosts. Subsequently we focus on the recently published transcriptomics of monocotyledonous plant responses looking at specific metabolic changes and their role during plant–nematode interactions. Insights that may be learned from nematode interactions with dicotyledonous hosts are also discussed. As a final point, we look at nematode effectors during monocots–nematode interactions exploiting de novo transcriptome data produced from root-knot nematodes and cyst nematodes.

Introduction

Among flowering plants (Angiosperms) monocotyledons have been separated from dicotyledons based on morphological features particularly because the embryo is formed from one cotyledon in the former versus two cotyledons in the latter (Jussieu, 1789). Another morphological aspect differing among them is that monocots have adventitious roots that arise from stem nodes, after development of the seminal root system. Nodal roots are thicker, and are associated with tiller development. The root vascular system organization also differs in monocots, with the presence of a central metaxylem vessel in the stele, surrounded by alternate bands of xylem and phloem (Esau, 1953).

Based on molecular studies, monocotyledons form a well-separated monophyletic clade comprising 10 orders (and two families not yet assigned) (APG III system (Angiosperm Phylogeny Group III system)) of flowering plant classification (Angiosperm Phylogeny Group, 2009). The largest families of monocotyledons are the orchids, followed by the Poaceae, also called Gramineae or true grasses, being the fifth largest plant family. Other important monocots are the palm (Arecaceae), banana (Musaceae), ginger (Zingiberaceae) and the amaryllis (Amaryllidaceae) families. The latter includes ornamental plants cultivated for their blossom, notably lilies, amaryllis and tulips as well as ubiquitously consumed vegetables as onions and garlic.

Monocotyledons include economically important species, like sugar cane (Saccharum officinarum), and cultivated grains (cereals), including rice (Oryza sativa), wheat (Triticum aestivum; Triticum durum), maize (Zea maïs), sorghum (Sorghum bicolor) and others. Within the 20 most important food and agricultural commodities in the world (2012), rice is classified together with milk and meat (cattle, pig and chicken) (FAOSTAT, 2013, http://issuu.com/faooftheun/docs/syb2013issuu). Subsequently come wheat, sugar cane, maize, banana and cassava, listed together with other eight dicotyledonous crops. Monocot crops comprise 40% of the total cultivated area in the world, and cereals (e.g. wheat, maize, rice), starchy roots (cassava, yams) and fruits (banana and plantain) are the main source of carbohydrates for human and animal consumption. Cereals have been cultivated for their edible seeds and are an important part of the man diet worldwide. Sugar cane, an important source for sugar (sucrose) in the human diet, is now also extensively cultivated for biofuel (ethanol) production. Other monocotyledonous species providing carbohydrate or oils as food source include the date palm (Phoenix dactylifera), oil palm (Elaeis guineensis), coconut and other palm species. In addition to edible types monocots are cultivated as ornamentals, including turfgrasses, also widely used in many private and public lawns contributing to agro-economical sources. Finally, wild monocot species are weeds frequently acting as reservoirs for many plant pathogens.

Diseases caused by nematodes in monocots are well documented, and a series of exhaustive reviews about nematode parasites of bananas (Gowen, Quénéhervé, & Fogain, 2005), cereals (Bridge et al., 2005, Mc Donald and Nicol, 2005), palms (Griffith, Giblin-Davis, Koshy, & Sossama, 2005), pineapple (Sipes, Caswell-Chen, Sarah, & Apt, 2005) and sugar cane (Cadet & Spaull, 2005) have been compiled in a book focused on tropical and subtropical crop species (Luc, Sikora, & Bridge, 2005). However, in spite of their widespread occurrence and high abundance, only few data are available on monocot–nematode interactions (Kyndt, Fernandez, & Gheysen, 2014). Efforts have been made to control widespread pathogenic nematodes in banana and plantains (Musa spp.) severely affecting crop productivity and longevity (extensively reviewed in Quénéhervé, 2009). Among the most important root pathogens of banana are the burrowing nematode Radopholus similis and some species of the root lesion nematode Pratylenchus spp. These species attack primary roots disrupting the anchorage system resulting in host plant toppling or uprooting. Production losses due to attacks by these nematode species can be high, also depending on other biotic and environmental factors (Quénéhervé, 2009). In addition, root-knot nematodes (RKN) belonging to the Meloidogyne genus, may also infect all banana varieties causing root deformations and stunting. Until the 1990s, control of nematode attacks on banana relied almost exclusively on the regular application of nematicides. However, as pointed out by Quénéhervé (2009), ‘the golden age of chemical control with nematicides is definitely behind us’ and different approaches to nematode management (e.g. cultural practices, plant resistance and biological control) must be used depending on each cropping systems. Owing to national and international efforts during the last 50 years, fundamental data have been generated on nematodes attacking important crops like bananas and plantains and new nematode management practices have been put in action.

It is therefore of crucial importance to identify novel sources of natural resistance to nematodes in crop species as well also to investigate more deeply plant–nematode interactions, including plant defence mechanisms and nematode manipulation of the host cell metabolism. Enhancing our basic knowledge on plant–nematode interactions may help defining future strategies for contributing to best plant health measures. Most of the available studies on the molecular interplay between plants and nematodes come from dicots (Kyndt, Vieira, Gheysen, & de Almeida-Engler, 2013). Therefore, the purpose of this review is to present up to date data and to identify major trends in plant–nematode interactions in monocots. As well we survey here and discuss in more detail existing histological and molecular data on the interaction of monocots and sedentary nematodes of the suborder Tylenchina.

Section snippets

Monocotyledonous Plant–Nematode Systems: Biology and Genetics of Interactions

RKN and cyst nematodes (CN) are both obligate sedentary endoparasites. In order to complete their life cycle, they must invade the roots of a susceptible plant where they induce a specialized nematode-feeding site, called syncytium for CN or giant cells for RKN. These specialized feeding structures serve as a constant food source to the nematode, allowing its development into a reproductive female (Kyndt et al., 2013). CN females mature into cysts that contain several hundred eggs, whereas RKN

Histological Descriptions of Roots during Nematode Development and Host Resistance Responses

Histology of gall development during RKN infection in monocotyledonous plants has been investigated in banana, date palms, ginger, rice, sorghum, wheat and barley and in some of their relative wild species, and finally, turfgrasses (Table 1). However, only one study refers to CN in monocots that describes the development of the CCN (H. avenae) in susceptible and resistant wheat varieties (Seah, Miller, Sivasithamparam, & Lagudah, 2000). A large amount of reported data refer to M. naasi, an RKN

Transcriptomics of Monocotyledonous Plant Responses to Nematodes

Using transcriptome analyses, the response of a plant upon infection with nematodes can be efficiently monitored, leading to insights into the pathways that are (1) manipulated by the pathogen or (2) activated/suppressed by the plant as a defence response.

An RNA-Seq analysis of the incompatible interaction between A. variabilis and CCNs (Xu et al., 2013) analysed a pooled RNA sample to construct a de novo transcriptome of both infected and uninfected Aegilops roots at three time points, 30 hpi,

Nematode Effectors in Monocots–Nematode Interactions

A key feature of sedentary plant-parasitic nematodes is the release of effector proteins secreted from their oesophageal gland cells through their stylet into host roots, so they can manipulate the cellular machinery and transform parenchymatic vascular cells in feeding sites (Hewezi & Baum, 2013). Transcriptomic and proteomic approaches identified putative secreted protein sequences from various nematode developmental stages or tissues, and from mixed samples of plant–nematode-infected tissues

Conclusions

Our understanding of the biological and molecular processes in monocot plant–nematode interactions is still fragmentary; however, new data show that common mechanisms act in monocot and dicot plant–nematode interactions. We highlighted some specific features in the developmental RKN cycle that are different from other RKN species attacking dicotyledons. New effector genes will soon be identified in some of the most studied RKN species adapted to graminaceous hosts. Transcriptome data have

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    a

    NVP was recipient of a Vietnamese governmental PhD grant and MGS of a PhD grant from the Conselho Nacional de Desenvolvimento Cientifico e Tecnológico (CNPq-CSF) in Brazil.

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    Tina Kyndt is supported by a postdoctoral fellowship from the Fonds Wetenschappelijk Onderzoek–Vlaanderen (FWO) in Belgium.

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