Involvement of NAC transcription factor NaNAC29 in Alternaria alternata resistance and leaf senescence in Nicotiana attenuata

doi:10.1016/j.pld.2020.11.003

Plant Diversity ›› 2021, Vol. 43 ›› Issue (06): 502-509.DOI: 10.1016/j.pld.2020.11.003

Involvement of NAC transcription factor NaNAC29 in Alternaria alternata resistance and leaf senescence in Nicotiana attenuata

Lan Ma^a, Rongping Li^a,b, Luoyan Ma^a, Na Song^a,b, Zhen Xu^a,b, Jinsong Wu^a

a Yunnan Key Laboratory for Wild Plant Resources, Kunming Institute of Botany, Chinese Academy of Sciences, Lanhei Road 132, 650201, Kunming, China;
b University of Chinese Academy of Science, Beijing 100049, China

收稿日期:2020-09-01 修回日期:2020-10-16 出版日期:2021-12-25 发布日期:2022-01-11
通讯作者: Lan Ma, Jinsong Wu
基金资助:
We thank Biological Technology Open Platform of Kunming Institute of Botany, the Chinese Academy of Sciences for greenhouse services. This project is supported by CAS "Light of West China" Program and NSFC grant (No. 31700231) to LM.

Involvement of NAC transcription factor NaNAC29 in Alternaria alternata resistance and leaf senescence in Nicotiana attenuata

Lan Ma^a, Rongping Li^a,b, Luoyan Ma^a, Na Song^a,b, Zhen Xu^a,b, Jinsong Wu^a

a Yunnan Key Laboratory for Wild Plant Resources, Kunming Institute of Botany, Chinese Academy of Sciences, Lanhei Road 132, 650201, Kunming, China;
b University of Chinese Academy of Science, Beijing 100049, China

Received:2020-09-01 Revised:2020-10-16 Online:2021-12-25 Published:2022-01-11
Contact: Lan Ma, Jinsong Wu
Supported by:
We thank Biological Technology Open Platform of Kunming Institute of Botany, the Chinese Academy of Sciences for greenhouse services. This project is supported by CAS "Light of West China" Program and NSFC grant (No. 31700231) to LM.

摘要/Abstract

摘要： NAC-LIKE, ACTIVATED BY AP3/PI (NAP) is a NAC transcription factor regulating leaf senescence in Arabidopsis thaliana. In wild tobacco Nicotiana attenuata, a nuclear localized NAC transcription factor NaNAC29 was identified to be highly elicited after inoculation of Alternaria alternata, a notorious necrotic fungus on tobacco species. The NaNAC29 possesses similar tertiary structure to NAP with 60% amino acid identity. However, it remains unknown the role of NaNAC29 in plant defense responses to A. alternata and leaf senescence in N. attenuata. In this paper, Defensin-like protein 1 (NaDLP1) was highly induced in N. attenuata after A. alternata inoculation and bigger lesions were developed in NaDLP1-silenced plants. Interestingly, A. alternata-induced NaDLP1 was reduced by 76% in VIGS NaNAC29 plants and by 61% in JA deficient irAOC plants at 3 days post inoculation. The regulation of NaDLP1 expression by NaNAC29 was clearly independent on JA pathway, since exogenous methyl jasmonate treatment could not complement the induction levels of NaDLP1 in NaNAC29-silenced plants to the levels in WT plants. Otherwise, the expression of NaNAC29 was low expressed in young leaves but highly in senescent leaves and darktreated leaves. NaNAC29-silenced plants, which were generated by virus-induced gene silencing (VIGS NaNAC29), showed delayed senescence phenotype. In addition, constitutive over-expression of NaNAC29 in A. thaliana could rescue the delayed-senescence phenotype of nap and caused precocious leaf senescence of wild-type Col-0 plants. All the data above demonstrate that NaNAC29 is a NAP homolog in N. attenuata participating in the defense responses to A. alternata by regulation of a defensin protein NaDLP1 and promoting leaf senescence.

关键词: NaNAC29, Defensin-like protein 1, Tobacco, Brown spot disease, Aging

Abstract: NAC-LIKE, ACTIVATED BY AP3/PI (NAP) is a NAC transcription factor regulating leaf senescence in Arabidopsis thaliana. In wild tobacco Nicotiana attenuata, a nuclear localized NAC transcription factor NaNAC29 was identified to be highly elicited after inoculation of Alternaria alternata, a notorious necrotic fungus on tobacco species. The NaNAC29 possesses similar tertiary structure to NAP with 60% amino acid identity. However, it remains unknown the role of NaNAC29 in plant defense responses to A. alternata and leaf senescence in N. attenuata. In this paper, Defensin-like protein 1 (NaDLP1) was highly induced in N. attenuata after A. alternata inoculation and bigger lesions were developed in NaDLP1-silenced plants. Interestingly, A. alternata-induced NaDLP1 was reduced by 76% in VIGS NaNAC29 plants and by 61% in JA deficient irAOC plants at 3 days post inoculation. The regulation of NaDLP1 expression by NaNAC29 was clearly independent on JA pathway, since exogenous methyl jasmonate treatment could not complement the induction levels of NaDLP1 in NaNAC29-silenced plants to the levels in WT plants. Otherwise, the expression of NaNAC29 was low expressed in young leaves but highly in senescent leaves and darktreated leaves. NaNAC29-silenced plants, which were generated by virus-induced gene silencing (VIGS NaNAC29), showed delayed senescence phenotype. In addition, constitutive over-expression of NaNAC29 in A. thaliana could rescue the delayed-senescence phenotype of nap and caused precocious leaf senescence of wild-type Col-0 plants. All the data above demonstrate that NaNAC29 is a NAP homolog in N. attenuata participating in the defense responses to A. alternata by regulation of a defensin protein NaDLP1 and promoting leaf senescence.

Key words: NaNAC29, Defensin-like protein 1, Tobacco, Brown spot disease, Aging

Lan Ma, Rongping Li, Luoyan Ma, Na Song, Zhen Xu, Jinsong Wu. Involvement of NAC transcription factor NaNAC29 in Alternaria alternata resistance and leaf senescence in Nicotiana attenuata[J]. Plant Diversity, 2021, 43(06): 502-509.

参考文献

Allu, A.D., Brotman, Y., Xue, G.P., et al., 2016. Transcription factor ANAC032 modulates JA/SA signalling in response to Pseudomonas syringae infection. EMBO Rep. 17, 1578-1589. https://doi.org/10.15252/embr.201642197.
Anderson FTLaMA, 2005. Defensins e components of the innate immune system in plants. Curr. Protein Pept. Sci. 6, 85-101.
Chen, Y., Qiu, K., Kuai, B., et al., 2011. Identification of an NAP-like transcription factor BeNAC1 regulating leaf senescence in bamboo (Bambusa emeiensis’Viridiflavus’). Physiol. Plantarum 142, 361-371. https://doi.org/10.1111/j.1399-3054.2011.01472.x.
Fan, K., Bibi, N., Gan, S., et al., 2015. A novel NAP member GhNAP is involved in leaf senescence in Gossypium hirsutum. J. Exp. Bot. 66, 4669-4682. https://doi.org/10.1093/jxb/erv240.
Frank, R., Am M-H, Dc B, 2001. Technical advance. Tobacco rattle virus as a vector for analysis of gene function by silencing. Plant J. 25, 237-245.
Greco, M., Chiappetta, A., Bruno, L., et al., 2012. Arabidopsis ATNAP regulates fruit senescence. J. Exp. Bot. 63, 695-709. https://doi.org/10.1093/jxb/err313.
Guo, Y., Gan, S., 2006. AtNAP, a NAC family transcription factor, has an important role in leaf senescence. Plant J. 46, 601-612. https://doi.org/10.1111/j.1365-313X.2006.02723.x.
He, X., Jiang, J., Wang, C.Q., et al., 2017. ORA59 and EIN3 interaction couples jasmonate-ethylene synergistic action to antagonistic salicylic acid regulation of PDF expression. J. Integr. Plant Biol. 59, 275-287. https://doi.org/10.1111/jipb.12524.
Huang, Q., Wang, Y., Li, B., et al., 2015. TaNAC29, a NAC transcription factor from wheat, enhances salt and drought tolerance in transgenic Arabidopsis. BMC Plant Biol. 15, 268. https://doi.org/10.1186/s12870-015-0644-9.
Kallenbach, M., Bonaventure, G., Gilardoni, P.A., et al., 2012. Empoasca leafhoppers attack wild tobacco plants in a jasmonate-dependent manner and identify jasmonate mutants in natural populations. Proc. Natl. Acad. Sci. U.S.A. 109, E1548-E1557. https://doi.org/10.1073/pnas.1200363109.
Kou, X., Liu, C., Han, L., et al., 2016. NAC transcription factors play an important role in ethylene biosynthesis, reception and signaling of tomato fruit ripening. Mol.Genet. Genom. 291 (3), 1205-1217. https://doi.org/10.1007/s00438-016-1177-0.
Kovalchuk, N., Wu, W., Bazanova, N., et al., 2019. Wheat wounding-responsive HDZip IV transcription factor GL7 is predominantly expressed in grain and activates genes encoding defensins. Plant Mol. Biol. 101, 41-61. https://doi.org/10.1007/s11103-019-00889-9.
Lacerda, A.F., Vasconcelos, E.A., Pelegrini, P.B., et al., 2014. Antifungal defensins and their role in plant defense. Front. Microbiol. 5, 116. https://doi.org/10.3389/fmicb.2014.00116.
LaMondia, J.A., 2001. Outbreak of brown spot of tobacco caused by Alternaria alternata in Connecticut and Massachusetts. Plant Dis. 85, 230. https://doi.org/10.1094/PDIS.2001.85.2.230B.
Li, W., Li, X., Chao, J., et al., 2018. NAC family transcription factors in tobacco and their potential role in regulating leaf senescence. Front. Plant Sci. 9, 1900.https://doi.org/10.3389/fpls.2018.01900.
Li, Y., Sorefan, K., Hemmann, G., Bevan, M.W., 2004. Arabidopsis NAP and PIR regulate actin-based cell morphogenesis and multiple developmental processes. Plant Physiol. 136, 3616-3627. https://doi.org/10.1104/pp.104.053173.
Li, S., Zhang, J., Liu, H., et al., 2019. Dodder-transmitted mobile signals prime host plants for enhanced salt tolerance. J. Exp. Bot. https://doi.org/10.1093/jxb/erz481.
Nakashima, K., Takasaki, H., Mizoi, J., et al., 2012. NAC transcription factors in plant abiotic stress responses. Biochim. Biophys. Acta 1819, 97-103. https://doi.org/10.1016/j.bbagrm.2011.10.005.
Nakashima, K., Tran, L.S., Van Nguyen, D., et al., 2007. Functional analysis of a NACtype transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. Plant J. 51 (4), 617-630. https://doi.org/10.1111/j.1365-313X.2007.03168.x.
Ndamukong, I., Abdallat, A.A., Thurow, C., et al., 2007. SA-inducible Arabidopsis glutaredoxin interacts with TGA factors and suppresses JA-responsive PDF1.2 transcription. Plant J. 50 (1), 128-139. https://doi.org/10.1111/j.1365-313X.2007.03039.x.
Pre, M., Atallah, M., Champion, A., et al., 2008. The AP2/ERF domain transcription factor ORA59 integrates jasmonic acid and ethylene signals in plant defense.Plant Physiol. 147 (3), 1347-1357. https://doi.org/10.1104/pp.108.117523.
Ren, T., Wang, J., Zhao, M., et al., 2018. Involvement of NAC transcription factor SiNAC1 in a positive feedback loop via ABA biosynthesis and leaf senescence in foxtail millet. Planta 247 (1), 53-68. https://doi.org/10.1007/s00425-017-2770-0.
Saedler, R., Baldwin, I.T., 2004. Virus-induced gene silencing of jasmonate-induced direct defences, nicotine and trypsin proteinase-inhibitors in Nicotiana attenuata. J. Exp. Bot. 55, 151-157. https://doi.org/10.1093/jxb/erh004.
Sathoff, A.E., Samac, D.A., 2019. Antibacterial activity of plant defensins. Mol. Plant Microbe Interact. 32 (5), 507-514. https://doi.org/10.1094/MPMI-08-18-0229-CR.
Seok, H.-Y., Woo, D.-H., Nguyen, L.V., et al., 2016. Arabidopsis AtNAP functions as a negative regulator via repression of AREB1 in salt stress response. Planta 245(2), 329-341. https://doi.org/10.1007/s00425-016-2609-0.
Shen, G., Pang, Y., Wu, W., et al., 2005. Molecular cloning, characterization and expression of a novel jasmonate-dependent defensin gene from Ginkgo biloba. J. Plant Physiol. 162 (10), 1160-1168. https://doi.org/10.1016/j.jplph.2005.01.019.
Song, N., Ma, L., Wang, W., et al., 2019. An ERF2-like transcription factor regulates production of the defense sesquiterpene capsidiol upon Alternaria alternata infection. J. Exp. Bot. 70 (20), 5895-5908. https://doi.org/10.1093/jxb/erz327.
Sun, H., Hu, X., Ma, J., Hettenhausen, C., Wang, L., Sun, G., Wu, J., Wu, J., 2014a. Requirement of ABA signalling-mediated stomatal closure for resistance of wild tobacco to Alternaria alternata. Plant Pathol. 63, 1070-1077. https://doi.org/10.1111/ppa.12181.
Sun, H., Song, N., Ma, L., et al., 2017. Ethylene signalling is essential for the resistance of Nicotiana attenuata against Alternaria alternata and phytoalexin scopoletin biosynthesis. Plant Pathol. 66, 277-284. https://doi.org/10.1111/ppa.12568.
Sun, H., Wang, L., Zhang, B., Ma, J., Hettenhausen, C., Cao, G., Sun, G., Wu, J., Wu, J., 2014b. Scopoletin is a phytoalexin against Alternaria alternata in wild tobacco dependent on jasmonate signalling. J. Exp. Bot. 65 (15), 4305-4315. https://doi.org/10.1093/jxb/eru203.
Thevissen, K., Ferket, K.K., Francois, I.E., et al., 2003. Interactions of antifungal plant defensins with fungal membrane components. Peptides 24 (11), 1705-1712.https://doi.org/10.1016/j.peptides.2003.09.014.
van der Weerden, N.L., Hancock, R.E., Anderson, M.A., 2010. Permeabilization of fungal hyphae by the plant defensin NaD1 occurs through a cell wall-dependent process. J. Biol. Chem. 285 (48), 37513-37520. https://doi.org/10.1074/jbc.M110.134882.
van der Weerden, N.L., Lay, F.T., Anderson, M.A., 2008. The plant defensin, NaD1, enters the cytoplasm of Fusarium oxysporum hyphae. J. Biol. Chem. 283 (21), 14445-14452. https://doi.org/10.1074/jbc.M709867200.
von Dahl, C.C., Winz, R.A., Halitschke, R., et al., 2007. Tuning the herbivore-induced ethylene burst: the role of transcript accumulation and ethylene perception in Nicotiana attenuata. Plant J. 51 (2), 293-307. https://doi.org/10.1111/j.1365-313X.2007.03142.x.
Vroemen, C.W., Mordhorst, A.P., Albrecht, C., et al., 2003. The CUP-SHAPED COTYLEDON3 gene is required for boundary and shoot meristem formation in Arabidopsis. Plant Cell 15 (7), 1563-1577. https://doi.org/10.1105/tpc.012203.
Weaver, L.M., Amasino, R.M., 2001. Senescence is induced in individually darkened Arabidopsis leaves, but inhibited in whole darkened plants. Plant Physiol. 127(3), 876-886. https://doi.org/10.1104/pp.010312.
Xu, Z., Song, N., Ma, L., et al., 2018. NaPDR1 and NaPDR1-like are essential for the resistance of Nicotiana attenuata against fungal pathogen Alternaria alternata. Plant Divers. 40, 68-73. https://doi.org/10.1016/j.pld.2018.01.001.
Yamaguchi, M., Ohtani, M., Mitsuda, N., et al., 2010. VND-INTERACTING2, a NAC domain transcription factor, negatively regulates xylem vessel formation in Arabidopsis. Plant Cell 22, 1249-1263. https://doi.org/10.1105/tpc.108.064048.
Yan, H., Zhang, A., Ye, Y., et al., 2017. Genome-wide survey of switchgrass NACs family provides new insights into motif and structure arrangements and reveals stress-related and tissue-specific NACs. Sci. Rep. 7, 3056. https://doi.org/10.1038/s41598-017-03435-z.
Yang, J., Worley, E., Udvardi, M., 2014. A NAP-AAO3 regulatory module promotes chlorophyll degradation via ABA biosynthesis in Arabidopsis leaves. Plant Cell 26, 4862-4874. https://doi.org/10.1105/tpc.114.133769.
Zhang, K., Gan, S.S., 2012. An abscisic acid-AtNAP transcription factor-SAG113 protein phosphatase 2C regulatory chain for controlling dehydration in senescing Arabidopsis leaves. Plant Physiol. 158, 961-969. https://doi.org/10.1104/pp.111.190876.

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Involvement of NAC transcription factor NaNAC29 in Alternaria alternata resistance and leaf senescence in Nicotiana attenuata

Involvement of NAC transcription factor NaNAC29 in Alternaria alternata resistance and leaf senescence in Nicotiana attenuata

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