Potential Molecular Mimicry Proteins Responsive to α-pinene in Bursaphelenchus xylophilus

Abstract

Bursaphelenchus xylophilus is a nematode species that has damaged pine trees worldwide, but its pathogenesis has not been fully characterized. α-pinene helps protect host species during the early B. xylophilus infection and colonization stages. In this study, we identified potential molecular mimicry proteins based on a comparative transcriptomic analysis of B. xylophilus. The expression levels of three genes encoding secreted B. xylophilus proteins were influenced by α-pinene. We cloned one gene encoding a thaumatin-like protein, Bx-tlp-2 (accession number MK000287), and another gene encoding a cysteine proteinase inhibitor, Bx-cpi (accession number MK000288). Additionally, α-pinene appeared to induce Bx-tlp-1 expression, but had the opposite effect on Bx-cpi expression. An analysis of the expression of the potential molecular mimicry proteins in B. xylophilus infecting pine trees revealed that the α-pinene content was consistent with the expression levels of Bx-tlp-1 (Bx-cpi) and Pm-tlp (Pm-cpi) over time. Thus, these genes likely have important roles contributing to the infection of pine species by B. xylophilus. The results of this study may be relevant for future investigations of the functions of Bx-tlp-1, Bx-tlp-2 and Bx-cpi, which may provide a point to explore the relationship between B. xylophilus and host pines.

Thaumatin-like proteins and a cysteine protease inhibitor secreted by the pine wood nematode Bursaphelenchus xylophilus induce cell death in Nicotiana benthamiana

“…We previously reported that Bx-CPI is most similar to a cystatin-like peptidase inhibitor in the herbaceous plant Medicago truncatula [ 18 ]. However, Meng et al (2020) [ 40 ] reported that Bx-CPI is more similar to the CP inhibitor five-like protein of the common sunflower Helianthus annuus (XP_022033148.1), which shares 32.5% identity with this protein, with over 62% query coverage based on a BLAST analysis of the current database. Although the phylogenetic analysis showed that Bx-CPI clustered in the same clade with an unnamed Enterobius vermicularis (Oxyuridae) protein, no other nematode proteins were clustered to the same group [ 40 ].…”

“…It has been suggested that Bx-TH1, Bx-TH2, and Bx-CPI mimic host plant defense systems [ 18 ]. Although a very high level of similarity in the amino acid sequences between these PWN proteins and plant proteins was not observed, Wang et al [ 39 ] and Meng et al [ 40 ] suggested that the possible role of these PWN proteins is to mimic host pine defense systems based on the result of phylogenetic and structure prediction analyses. Molecular mimicry is among the best-known strategies for host–parasite defense system evasion and host manipulation.…”

“…The amino acid sequence of Bx-TH1 shares 32% identity with the thaumatin-like protein of Pinus monticola (ADB97933.1) [39], though no highly similar sequence (e-value < 1e -10 ) was found in all organisms. Meng et al (2020) [40] reported that Bx-TH2 is similar to the Hall's panicgrass Panicum hallii thaumatin-like protein (XP_025808117.1), and it shares 52.05% identity with this protein, with over 85% query coverage. In plants, thaumatin is induced by a variety of phytopathogens via salicylic acid [33,34].…”

“…However, Meng et al (2020) [40] reported that Bx-CPI is more similar to the CP inhibitor five-like protein of the common sunflower Helianthus annuus (XP_022033148.1), which shares 32.5% identity with this protein, with over 62% query coverage based on a BLAST analysis of the current database. Although the phylogenetic analysis showed that Bx-CPI clustered in the same clade with an unnamed Enterobius vermicularis (Oxyuridae) protein, no other nematode proteins were clustered to the same group [40]. Cystatin mainly inhibits peptidases in the C1 (papain) and C13 (legumain) peptidase families; however, it has multiple roles, including the control of endogenous cysteine peptidases, seed development, and programmed cell death (in which it acts as both the regulator and executioner) [45][46][47].…”

Recent studies on pinene and its biological and pharmacological activities

“…Herein, we summarize the recent published findings on the biological and pharmacological activities of pinene (Table 1 (Tab. 1) ; References in Table 1: Bouzenna et al, 2017[ 3 ]; Cardoso et al, 2020[ 4 ]; Chen et al, 2015[ 5 ]; de Macêdo et al, 2018[ 6 ]; do Amaral et al, 2020[ 7 ]; Ensaka and Sakamoto, 2020[ 8 ]; Felipe et al, 2019[ 10 ]; Govindarajan et al, 2016[ 11 ]; Hou et al, 2019[ 12 ]; İnce et al, 2018[ 13 ]; Jensen et al, 2020[ 14 ]; Jo et al, 2021[ 15 ]; Karthikeyan et al, 2018[ 17 ], 2019[ 16 ]; Kasuya et al, 2015[ 18 ]; Khoshnazar et al, 2019[ 19 ], 2020[ 20 ]; Kim et al, 2015[ 21 ]; Kovač et al, 2015[ 22 ]; Kusuhara et al, 2019[ 23 ]; Langsi et al, 2020[ 24 ]; Lee et al, 2017[ 25 ]; Li et al, 2016[ 28 ]; Memariani et al, 2017[ 29 ]; Meng et al, 2020[ 30 ]; Min et al, 2020[ 32 ]; Moreira et al, 2016[ 33 ]; Nóbrega et al, 2020[ 34 ]; Pajaro-Castro et al, 2017[ 35 ]; Pinheiro et al, 2015[ 36 ]; Porres-Martínez et al, 2016[ 37 ]; Rodrigues et al, 2015[ 39 ]; Šimunović et al, 2020[ 41 ]; Ueno et al, 2019[ 44 ], 2020[ 43 ]; Wang et al, 2019[ 46 ]; Xu et al, 2018[ 47 ]; Yang et al, 2016[ 48 ]; Zamyad et al, 2019[ 50 ]; Zhang et al, 2015[ 52 ], 202[ 51 ]0; Zhao et al, 2018[ 53 ]).…”