NbEXPA1, an α‐expansin, is plasmodesmata‐specific and a novel host factor for potyviral infection

Abstract

Plasmodesmata (PD), unique to the plant kingdom, are structurally complex microchannels that cross the cell wall to establish symplastic communication between neighbouring cells. Viral intercellular movement occurs through PD. To better understand the involvement of PD in viral infection, we conducted a quantitative proteomic study on the PD-enriched fraction from Nicotiana benthamiana leaves in response to infection by Turnip mosaic virus (TuMV). We report the identification of a total of 1070 PD protein candidates, of which 100 (≥2-fold increase) and 48 (≥2-fold reduction) are significantly differentially accumulated in the PD-enriched fraction, when compared with protein levels in the corresponding healthy control. Among the differentially accumulated PD protein candidates, we show that an α-expansin designated NbEXPA1, a cell wall loosening protein, is PD-specific. TuMV infection downregulates NbEXPA1 mRNA expression and protein accumulation. We further demonstrate that NbEXPA1 is recruited to the viral replication complex via the interaction with NIb, the only RNA-dependent RNA polymerase of TuMV. Silencing of NbEXPA1 inhibits plant growth and TuMV infection, whereas overexpression of NbEXPA1 promotes viral replication and intercellular movement. These data suggest that NbEXPA1 is a host factor for potyviral infection. This study not only generates a PD-proteome dataset that is useful in future studies to expound PD biology and PD-mediated virus-host interactions but also characterizes NbEXPA1 as the first PD-specific cell wall loosening protein and its essential role in potyviral infection.

Massive up‐regulation of LBD transcription factors and EXPANSINs highlights the regulatory programs of rhizomania disease

“…Among the factors studied during rhizomania development, EXP s are primarily known for their role in plant CW remodelling by breaking the hydrogen bonds between cellohexaose and pectin; they thus participate in various aspects of plant development involving cell division and expansion (Cosgrove, ), and as potential pro‐viral factors (Chen et al., ; Park et al., ). The data accumulated from studies in various plant pathosystems, including nematodes, fungi and viruses, suggest that the down‐regulation of EXP s may represent a defence response (Marowa et al., ).…”

“…In Arabidopsis , the down‐regulation or knockdown of AtEXLA2 enhances resistance to the necrotrophic fungus Alternaria brassicicola (Abuqamar et al., ). The knockdown of NbEXPA1 in N. benthamiana induces resistance to Turnip mosaic virus (TuMV) (Park et al., ). Furthermore, it has been shown that NbEXPA1 is a plasmodesmata‐specific protein recruited by TuMV to the virus replication complex through its interaction with the viral RNA‐dependent RNA polymerase, the NIb protein, and transient expression of NbEXPA1 promotes TuMV replication and cell‐to‐cell movement (Park et al., ).…”

“…The knockdown of NbEXPA1 in N. benthamiana induces resistance to Turnip mosaic virus (TuMV) (Park et al., ). Furthermore, it has been shown that NbEXPA1 is a plasmodesmata‐specific protein recruited by TuMV to the virus replication complex through its interaction with the viral RNA‐dependent RNA polymerase, the NIb protein, and transient expression of NbEXPA1 promotes TuMV replication and cell‐to‐cell movement (Park et al., ). Similarly, the knockdown of NbEXPA4 expression reduces Tobacco mosaic virus (TMV) accumulation in systemically infected plants, whereas the overexpression of NbEXPA4 accelerates virus replication (Chen et al., ).…”

Wheat Yellow Mosaic Virus NIb Interacting with Host Light Induced Protein (LIP) Facilitates Its Infection through Perturbing the Abscisic Acid Pathway in Wheat

“…It is possible that Nib-TaLIP interaction affects the function of TaLIP through changing the sub-cellular localization to facilitate WYMV infection. This assumption is supported by findings showing that TuMV NIb interacting with NbEXPA1 recruits NbEXPA1 to the viral replication complex and promotes TuMV infection [9]. Early study has shown that the negatively regulated ABA responses abscisic acid insensitive 2 (ABI2) interacts with the Arabidopsis FNB1a to regulate its localization, leading to perturbing the ABA pathway [36].…”

“…Potyviruses include many agriculturally and economically important pathogens such as Wheat yellow mosaic virus (WYMV), which belongs to the genus Bymovirus (Potyviridae) [8,9]. The WYMV genome consists of two positive single RNA strands, RNA1 (7.5 kb) and RNA2 (3.6 kb), which each encode a polyprotein [10].…”