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Study on aquaporins of Setaria italica suggests the involvement of SiPIP3;1 and SiSIP1;1 in abiotic stress response

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Abstract

Aquaporins are versatile proteins involved in several biological as well as molecular functions, and they have been extensively studied in various plant systems. Increasing evidences indicate their role in biotic and abiotic stresses, and therefore, studying these proteins in a naturally stress-tolerant crop would provide further insights into the roles of this important protein family. Given this, the present study was performed in foxtail millet (Setaria italica), a model plant for studying biofuel, stress tolerance, and C4 photosynthetic traits. The study identified 12 plasma membrane intrinsic proteins (PIPs), 11 tonoplast intrinsic proteins (TIPs), 13 NOD26-like intrinsic proteins (NIPs), and 3 small basic intrinsic proteins (SIPs) in foxtail millet. The identified proteins and their corresponding genes were characterized using in silico approaches such as chromosomal localization, analysis of gene and protein properties, phylogenetic analysis, promoter analysis, and RNA-seq-derived expression profiling. The candidate genes identified through these analyses were studied for their expression in response to abiotic stresses (dehydration, salinity, and heat) as well as hormone treatments (abscisic acid, methyl jasmonate, and salicylic acid) in two contrasting cultivars of foxtail millet. The study showed that SiPIP3;1 and SiSIP1;1 were differentially expressed in both the cultivars in response to stress and hormone treatments. Overexpression of these genes in a heterologous yeast system also demonstrated that the transgenic cells were able to tolerate dehydration as well as salt stress which suggests the involvement of these proteins in the tolerance mechanism. Overall, the present study provides insights into structure and organization of the aquaporin gene family in foxtail millet and highlights the potential candidate genes for further functional characterizations.

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Acknowledgments

RKS and RR acknowledge the Council of Scientific and Industrial Research and Department of Biotechnology, Government of India, India, respectively, for providing Research Fellowships. SS acknowledges the National Post-Doctoral Fellowship received from DST-SERB, Government of India, India. MM acknowledges the DST INSPIRE Faculty Award from Department of Science & Technology, Government of India, India. The authors are thankful to DBT-eLibrary Consortium (DeLCON) for providing access to the e-resources.

Funding

Authors’ research in this area is supported by the Core Grant of National Institute of Plant Genome Research, New Delhi, India.

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Author notes

  1. Roshan Kumar Singh, Shweta Shweta, Mehanathan Muthamilarasan and Rekha Rani contributed equally to this work.

Authors and Affiliations

  1. National Institute of Plant Genome Research, Aruna Asaf Ali Marg, New Delhi, 110067, India

    Roshan Kumar Singh, Shweta Shweta, Mehanathan Muthamilarasan, Rekha Rani & Manoj Prasad

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  1. Roshan Kumar Singh
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  2. Shweta Shweta
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  3. Mehanathan Muthamilarasan
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  4. Rekha Rani
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Contributions

Conception and design: MP; experimental analyses: RKS, SS, RR, and MM; interpretation of data: MM and RKS; writing, review and revision of manuscript: MM and RKS; study supervision: MP; all authors have read and approved the final manuscript.

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Correspondence to Manoj Prasad.

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Supplementary Figure S1

Exon-Intron structure of aquaporin genes. (PNG 698 kb)

High Resolution Image (TIF 1191 kb)

Supplementary Figure S2

Sub-cellular localization of aquaporin genes. (PNG 174 kb)

High Resolution Image (TIF 407 kb)

Supplementary Figure S3

Comparative physical map of aquaporin genes between foxtail millet (Si; Setaria italica) and green foxtail (Sv; Setaria viridis), Brachypodium (Bd; Brachypodium distachyon), sorghum (Sb; Sorghum bicolor), maize (Zm; Zea mays), rice (Os; Oryza sativa) and switchgrass (Panicum virgatum). Each block represents individual chromosome of each organism and the lines denote the corresponding orthologous genes. (JPG 3022 kb)

High Resolution Image (TIF 1446 kb)

Supplementary Table S1

List of primers used in the present study. (DOC 34 kb)

Supplementary Table S2

Properties of aquaporin genes identified in foxtail millet. (XLS 48 kb)

Supplementary Table S3

Summary of cis-regulatory elements present in aquaporin genes. (XLS 268 kb)

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Singh, R.K., Shweta, S., Muthamilarasan, M. et al. Study on aquaporins of Setaria italica suggests the involvement of SiPIP3;1 and SiSIP1;1 in abiotic stress response. Funct Integr Genomics 19, 587–596 (2019). https://doi.org/10.1007/s10142-018-00653-0

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