Proteomics Analysis Reveals That Caspase-Like and Metacaspase-Like Activities Are Dispensable for Activation of Proteases Involved in Early Response to Biotic Stress in Triticum aestivum L.

Balakireva, Anastasia V.; Deviatkin, Andrei A.; Zgoda, Victor G.; Kartashov, Maxim I.; Zhemchuzhina, Natalia S.; Dzhavakhiya, Vitaly G.; Golovin, Andrey V.; Zamyatnin, Andrey A.

doi:10.3390/ijms19123991

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Proteomics Analysis Reveals That Caspase-Like and Metacaspase-Like Activities Are Dispensable for Activation of Proteases Involved in Early Response to Biotic Stress in Triticum aestivum L.

Anastasia V. Balakireva

^1,†,

Andrei A. Deviatkin

^1,†

Victor G. Zgoda

²,

Maxim I. Kartashov

³,

Natalia S. Zhemchuzhina

³,

Vitaly G. Dzhavakhiya

³,

Andrey V. Golovin

^1,4

and

Andrey A. Zamyatnin, Jr.

^1,5,*

Sechenov First Moscow State Medical University, Institute of Molecular Medicine, Trubetskaya str., 8, bld. 2, Moscow 119991, Russia

Institute of Biomedical Chemistry, Pogodinskaya str., 10, bld. 8, Moscow 119121, Russia

All Russian Research Institute of Phytopathology, VNIIF, Bolshie Vyazemi, Odintsovsky distr., Moscow region 143050, Russia

⁴

Faculty of Bioengineering and Bioinformatics, Moscow State University, Moscow 119992, Russia

⁵

Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, Moscow 119992, Russia

Author to whom correspondence should be addressed.

^†

These authors contributed equally to this work.

Int. J. Mol. Sci. 2018, 19(12), 3991; https://doi.org/10.3390/ijms19123991

Received: 8 November 2018 / Revised: 4 December 2018 / Accepted: 8 December 2018 / Published: 11 December 2018

(This article belongs to the Special Issue Plant Proteomic Research 2.0)

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Abstract

Plants, including Triticum aestivum L., are constantly attacked by various pathogens which induce immune responses. Immune processes in plants are tightly regulated by proteases from different families within their degradome. In this study, a wheat degradome was characterized. Using profile hidden Markov model (HMMer) algorithm and Pfam database, comprehensive analysis of the T. aestivum genome revealed a large number of proteases (1544 in total) belonging to the five major protease families: serine, cysteine, threonine, aspartic, and metallo-proteases. Mass-spectrometry analysis revealed a 30% difference between degradomes of distinct wheat cultivars (Khakasskaya and Darya), and infection by biotrophic (Puccinia recondita Rob. ex Desm f. sp. tritici) or necrotrophic (Stagonospora nodorum) pathogens induced drastic changes in the presence of proteolytic enzymes. This study shows that an early immune response to biotic stress is associated with the same core of proteases from the C1, C48, C65, M24, M41, S10, S9, S8, and A1 families. Further liquid chromatography-mass spectrometry (LC-MS) analysis of the detected protease-derived peptides revealed that infection by both pathogens enhances overall proteolytic activity in wheat cells and leads to activation of proteolytic cascades. Moreover, sites of proteolysis were identified within the proteases, which probably represent targets of autocatalytic activation, or hydrolysis by another protease within the proteolytic cascades. Although predicted substrates of metacaspase-like and caspase-like proteases were similar in biotrophic and necrotrophic infections, proteolytic activation of proteases was not found to be associated with metacaspase-like and caspase-like activities. These findings indicate that the response of T. aestivum to biotic stress is regulated by unique mechanisms. View Full-Text

Keywords: degradome; wheat; cultivar; protease; papain-like cysteine protease (PLCP); subtilase; metacaspase; caspase-like; wheat leaf rust; Puccinia recondita; Stagonospora nodorum

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Balakireva, A.V.; Deviatkin, A.A.; Zgoda, V.G.; Kartashov, M.I.; Zhemchuzhina, N.S.; Dzhavakhiya, V.G.; Golovin, A.V.; Zamyatnin, A.A., Jr. Proteomics Analysis Reveals That Caspase-Like and Metacaspase-Like Activities Are Dispensable for Activation of Proteases Involved in Early Response to Biotic Stress in Triticum aestivum L. Int. J. Mol. Sci. 2018, 19, 3991. https://doi.org/10.3390/ijms19123991

AMA Style

Balakireva AV, Deviatkin AA, Zgoda VG, Kartashov MI, Zhemchuzhina NS, Dzhavakhiya VG, Golovin AV, Zamyatnin AA Jr. Proteomics Analysis Reveals That Caspase-Like and Metacaspase-Like Activities Are Dispensable for Activation of Proteases Involved in Early Response to Biotic Stress in Triticum aestivum L. International Journal of Molecular Sciences. 2018; 19(12):3991. https://doi.org/10.3390/ijms19123991

Chicago/Turabian Style

Balakireva, Anastasia V., Andrei A. Deviatkin, Victor G. Zgoda, Maxim I. Kartashov, Natalia S. Zhemchuzhina, Vitaly G. Dzhavakhiya, Andrey V. Golovin, and Andrey A. Zamyatnin Jr. 2018. "Proteomics Analysis Reveals That Caspase-Like and Metacaspase-Like Activities Are Dispensable for Activation of Proteases Involved in Early Response to Biotic Stress in Triticum aestivum L." International Journal of Molecular Sciences 19, no. 12: 3991. https://doi.org/10.3390/ijms19123991

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Proteomics Analysis Reveals That Caspase-Like and Metacaspase-Like Activities Are Dispensable for Activation of Proteases Involved in Early Response to Biotic Stress in Triticum aestivum L.

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