Extensive structural variation in the Bowman-Birk inhibitor family in common wheat (Triticum aestivum L.)
Abstract Background Bowman-Birk inhibitors (BBI) are a family of serine-type protease inhibitors that modulate endogenous plant proteolytic activities during different phases of development. They also inhibit exogenous proteases as a component of plant defense mechanisms, and their overexpression ca...
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| Format: | Article |
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BMC
2021-03-01
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| Series: | BMC Genomics |
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| Online Access: | https://doi.org/10.1186/s12864-021-07475-8 |
| _version_ | 1819174764085772288 |
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| author | Yucong Xie Karl Ravet Stephen Pearce |
| author_facet | Yucong Xie Karl Ravet Stephen Pearce |
| author_sort | Yucong Xie |
| collection | DOAJ |
| description | Abstract Background Bowman-Birk inhibitors (BBI) are a family of serine-type protease inhibitors that modulate endogenous plant proteolytic activities during different phases of development. They also inhibit exogenous proteases as a component of plant defense mechanisms, and their overexpression can confer resistance to phytophagous herbivores and multiple fungal and bacterial pathogens. Dicot BBIs are multifunctional, with a “double-headed” structure containing two separate inhibitory loops that can bind and inhibit trypsin and chymotrypsin proteases simultaneously. By contrast, monocot BBIs have a non-functional chymotrypsin inhibitory loop, although they have undergone internal duplication events giving rise to proteins with multiple BBI domains. Results We used a Hidden Markov Model (HMM) profile-based search to identify 57 BBI genes in the common wheat (Triticum aestivum L.) genome. The BBI genes are unevenly distributed, with large gene clusters in the telomeric regions of homoeologous group 1 and 3 chromosomes that likely arose through a series of tandem gene duplication events. The genomes of wheat progenitors also contain contiguous clusters of BBI genes, suggesting this family underwent expansion before the domestication of common wheat. However, the BBI gene family varied in size among different cultivars, showing this family remains dynamic. Because of these expansions, the BBI gene family is larger in wheat than other monocots such as maize, rice and Brachypodium. We found BBI proteins in common wheat with intragenic homologous duplications of cysteine-rich functional domains, including one protein with four functional BBI domains. This diversification may expand the spectrum of target substrates. Expression profiling suggests that some wheat BBI proteins may be involved in regulating endogenous proteases during grain development, while others were induced in response to biotic and abiotic stresses, suggesting a role in plant defense. Conclusions Genome-wide characterization reveals that the BBI gene family in wheat is subject to a high rate of homologous tandem duplication and deletion events, giving rise to a diverse set of encoded proteins. This information will facilitate the functional characterization of individual wheat BBI genes to determine their role in wheat development and stress responses, and their potential application in breeding. |
| first_indexed | 2024-12-22T20:44:09Z |
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| institution | Directory Open Access Journal |
| issn | 1471-2164 |
| language | English |
| last_indexed | 2024-12-22T20:44:09Z |
| publishDate | 2021-03-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Genomics |
| spelling | doaj.art-7852ce1060cc453f93208e7a548b42ec2022-12-21T18:13:15ZengBMCBMC Genomics1471-21642021-03-0122112110.1186/s12864-021-07475-8Extensive structural variation in the Bowman-Birk inhibitor family in common wheat (Triticum aestivum L.)Yucong Xie0Karl Ravet1Stephen Pearce2Department of Soil and Crop Sciences, Colorado State UniversityDepartment of Soil and Crop Sciences, Colorado State UniversityDepartment of Soil and Crop Sciences, Colorado State UniversityAbstract Background Bowman-Birk inhibitors (BBI) are a family of serine-type protease inhibitors that modulate endogenous plant proteolytic activities during different phases of development. They also inhibit exogenous proteases as a component of plant defense mechanisms, and their overexpression can confer resistance to phytophagous herbivores and multiple fungal and bacterial pathogens. Dicot BBIs are multifunctional, with a “double-headed” structure containing two separate inhibitory loops that can bind and inhibit trypsin and chymotrypsin proteases simultaneously. By contrast, monocot BBIs have a non-functional chymotrypsin inhibitory loop, although they have undergone internal duplication events giving rise to proteins with multiple BBI domains. Results We used a Hidden Markov Model (HMM) profile-based search to identify 57 BBI genes in the common wheat (Triticum aestivum L.) genome. The BBI genes are unevenly distributed, with large gene clusters in the telomeric regions of homoeologous group 1 and 3 chromosomes that likely arose through a series of tandem gene duplication events. The genomes of wheat progenitors also contain contiguous clusters of BBI genes, suggesting this family underwent expansion before the domestication of common wheat. However, the BBI gene family varied in size among different cultivars, showing this family remains dynamic. Because of these expansions, the BBI gene family is larger in wheat than other monocots such as maize, rice and Brachypodium. We found BBI proteins in common wheat with intragenic homologous duplications of cysteine-rich functional domains, including one protein with four functional BBI domains. This diversification may expand the spectrum of target substrates. Expression profiling suggests that some wheat BBI proteins may be involved in regulating endogenous proteases during grain development, while others were induced in response to biotic and abiotic stresses, suggesting a role in plant defense. Conclusions Genome-wide characterization reveals that the BBI gene family in wheat is subject to a high rate of homologous tandem duplication and deletion events, giving rise to a diverse set of encoded proteins. This information will facilitate the functional characterization of individual wheat BBI genes to determine their role in wheat development and stress responses, and their potential application in breeding.https://doi.org/10.1186/s12864-021-07475-8Protease inhibitorBowman-Birk inhibitorTandem duplicationBiotic stressWheat |
| spellingShingle | Yucong Xie Karl Ravet Stephen Pearce Extensive structural variation in the Bowman-Birk inhibitor family in common wheat (Triticum aestivum L.) BMC Genomics Protease inhibitor Bowman-Birk inhibitor Tandem duplication Biotic stress Wheat |
| title | Extensive structural variation in the Bowman-Birk inhibitor family in common wheat (Triticum aestivum L.) |
| title_full | Extensive structural variation in the Bowman-Birk inhibitor family in common wheat (Triticum aestivum L.) |
| title_fullStr | Extensive structural variation in the Bowman-Birk inhibitor family in common wheat (Triticum aestivum L.) |
| title_full_unstemmed | Extensive structural variation in the Bowman-Birk inhibitor family in common wheat (Triticum aestivum L.) |
| title_short | Extensive structural variation in the Bowman-Birk inhibitor family in common wheat (Triticum aestivum L.) |
| title_sort | extensive structural variation in the bowman birk inhibitor family in common wheat triticum aestivum l |
| topic | Protease inhibitor Bowman-Birk inhibitor Tandem duplication Biotic stress Wheat |
| url | https://doi.org/10.1186/s12864-021-07475-8 |
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