The Role of Programmed Cell Death Regulator LSD1 in Nematode-Induced Syncytium Formation.

Mateusz Matuszkiewicz,Marcin Filipecki,Stanislaw Karpiński,Carolina Escobar,Javier Cabrera,Miroslaw Sobczak

doi:10.3389/fpls.2018.00314

Mateusz Matuszkiewicz, Marcin Filipecki + Show 4 more

Open Access

https://doi.org/10.3389/fpls.2018.00314

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Abstract

Cyst-forming plant-parasitic nematodes are common pests of many crops. They inject secretions into host cells to induce the developmental and metabolic reprogramming that leads to the formation of a syncytium, which is the sole food source for growing nematodes. As in other host-parasite models, avirulence leads to rapid and local programmed cell death (PCD) known as the hypersensitive response (HR), whereas in the case of virulence, PCD is still observed but is limited to only some cells. Several regulators of PCD were analyzed to understand the role of PCD in compatible plant–nematode interactions. Thus, Arabidopsis plants carrying recessive mutations in LESION SIMULATING DISEASE1 (LSD1) family genes were subjected to nematode infection assays with juveniles of Heterodera schachtii. LSD1 is a negative and conditional regulator of PCD, and fewer and smaller syncytia were induced in the roots of lsd1 mutants than in wild-type Col-0 plants. Mutation in LSD ONE LIKE2 (LOL2) revealed a pattern of susceptibility to H. schachtii antagonistic to lsd1. Syncytia induced on lsd1 roots compared to Col0 showed significantly retarded growth, modified cell wall structure, increased vesiculation, and some myelin-like bodies present at 7 and 12 days post-infection. To place these data in a wider context, RNA-sequencing analysis of infected and uninfected roots was conducted. During nematode infection, the number of transcripts with changed expression in lsd1 was approximately three times smaller than in wild-type plants (1440 vs. 4206 differentially expressed genes, respectively). LSD1-dependent PCD in roots is thus a highly regulated process in compatible plant–nematode interactions. Two genes identified in this analysis, coding for AUTOPHAGY-RELATED PROTEIN 8F and 8H were down-regulated in syncytia in the presence of LSD1 and showed an increased susceptibility to nematode infection contrasting with lsd1 phenotype. Our data indicate that molecular regulators belonging to the LSD1 family play an important role in precise balancing of diverse PCD players during syncytium development required for successful nematode parasitism.

Highlights

The development of feeding structures such as syncytia and giant cells, which are induced in plant roots upon infection with cystforming and root-knot nematodes, respectively, is a very complex process
To determine if Programmed cell death (PCD) regulators were involved in the development of feeding structures in Arabidopsis roots, infection tests were performed in loss of function lines of the LESION SIMULATING DISEASE1 (LSD1) gene family
A slight effect was seen in Ws0 background plants at 90 μmol m−2 s−1 which was best visualized as a comparison of female/male proportion, which was 1.21 in Ws0 and 0.93 in lsd1 mutants

Summary

Introduction

The development of feeding structures such as syncytia and giant cells, which are induced in plant roots upon infection with cystforming and root-knot nematodes, respectively, is a very complex process. A number of effectors have been described for both cyst and root-knot nematodes (Mitchum et al, 2013; Quentin et al, 2013; Evesvan den Akker et al, 2014; Niu et al, 2016; Mantelin et al, 2017); for example, infective juveniles of Heterodera schachtii secrete HsCLE1 and two effectors (CLAVATA 1 and 2-like genes) that modify hormone homeostasis (Wang et al, 2011), Hs4F01, which changes the defense response by manipulation of an oxidoreductase of the 2OG-Fe(II) oxygenase family (Patel et al, 2010); and Hs25A01, which modifies plant growth by interacting with chalcone synthase and the translation initiation factor eIF2β subunit (eIF-2bs) (Pogorelko et al, 2016)

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