Abstract
The family of aquaporins (AQPs), or major intrinsic proteins (MIPs), includes integral membrane proteins that function as transmembrane channels for water and other small molecules of physiological significance. MIPs are classified into five subfamilies in higher plants, including plasma membrane (PIPs), tonoplast (TIPs), NOD26-like (NIPs), small basic (SIPs) and unclassified X (XIPs) intrinsic proteins. This study reports a genome-wide survey of MIP encoding genes in sweet orange (Citrus sinensis L. Osb.), the most widely cultivated Citrus spp. A total of 34 different genes encoding C. sinensis MIPs (CsMIPs) were identified and assigned into five subfamilies (CsPIPs, CsTIPs, CsNIPs, CsSIPs and CsXIPs) based on sequence analysis and also on their phylogenetic relationships with clearly classified MIPs of Arabidopsis thaliana. Analysis of key amino acid residues allowed the assessment of the substrate specificity of each CsMIP. Gene structure analysis revealed that the CsMIPs possess an exon-intron organization that is highly conserved within each subfamily. CsMIP loci were precisely mapped on every sweet orange chromosome, indicating a wide distribution of the gene family in the sweet orange genome. Investigation of their expression patterns in different tissues and upon drought and salt stress treatments, as well as with ‘Candidatus Liberibacter asiaticus’ infection, revealed a tissue-specific and coordinated regulation of the different CsMIP isoforms, consistent with the organization of the stress-responsive cis-acting regulatory elements observed in their promoter regions. A special role in regulating the flow of water and nutrients is proposed for CsTIPs and CsXIPs during drought stress, and for most CsMIPs during salt stress and the development of HLB disease. These results provide a valuable reference for further exploration of the CsMIPs functions and applications to the genetic improvement of both abiotic and biotic stress tolerance in citrus.
Highlights
Aquaporins (AQPs) are integral membrane proteins that assist the rapid movement of water as well as other low molecular weight molecules across cellular membranes [1,2,3]
While a small number of different AQPs have been identified (2 in E. coli, 9 in S. cerevisiae, 11 in C. elegans and 13 in mammals [4]), a surprisingly large number of major intrinsic proteins (MIPs) homologues have been found in plants; for example, AQPs were found in Arabidopsis [5], in Zea mays [6], 33 in Oryza sativa [7], 28 in Vitis vinifera [8], 55 in Populus trichocarpa [9], 71 in Gossypium hirsutum [10], 47 in Solanum lycopersicum [11] and 66 in Glycine max [12]
The C. sinensis MIPs (CsMIPs) were classified in five different subfamilies, PIPs, TIPs, NIPs, SIPs and X intrinsic proteins (XIPs), based on analysis of the amino acid residues located in seven key positions (P1 to P7) that were previously proposed [12,34,35] to discriminate the different subfamilies (S2 Table), as well as on their phylogenetic relationships with the well classified MIPs of A. thaliana and XIPs of R. communis and N. benthamiana (S1 Fig)
Summary
Aquaporins (AQPs) are integral membrane proteins that assist the rapid movement of water as well as other low molecular weight molecules across cellular membranes [1,2,3]. While a small number of different AQPs have been identified (2 in E. coli, 9 in S. cerevisiae, 11 in C. elegans and 13 in mammals [4]), a surprisingly large number of MIP homologues have been found in plants; for example, AQPs were found in Arabidopsis [5], in Zea mays [6], 33 in Oryza sativa [7], 28 in Vitis vinifera [8], 55 in Populus trichocarpa [9], 71 in Gossypium hirsutum [10], 47 in Solanum lycopersicum [11] and 66 in Glycine max [12] These observations highlight a major role for plant MIPs as key regulators of the intricate flows of water and solutes required for growth and adaptive responses to the ever-changing environment. These findings suggest that the family of plant MIPs is larger and much more complex than previously anticipated and, may play critical roles in a wide range of biological processes that go far beyond the current knowledge
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