Developmental and Environmental Regulation of Aquaporin Gene Expression across Populus Species: Divergence or Redundancy?

Abstract

Aquaporins (AQPs) are membrane channels belonging to the major intrinsic proteins family and are known for their ability to facilitate water movement. While in Populus trichocarpa, AQP proteins form a large family encompassing fifty-five genes, most of the experimental work focused on a few genes or subfamilies. The current work was undertaken to develop a comprehensive picture of the whole AQP gene family in Populus species by delineating gene expression domain and distinguishing responsiveness to developmental and environmental cues. Since duplication events amplified the poplar AQP family, we addressed the question of expression redundancy between gene duplicates. On these purposes, we carried a meta-analysis of all publicly available Affymetrix experiments. Our in-silico strategy controlled for previously identified biases in cross-species transcriptomics, a necessary step for any comparative transcriptomics based on multispecies design chips. Three poplar AQPs were not supported by any expression data, even in a large collection of situations (abiotic and biotic constraints, temporal oscillations and mutants). The expression of 11 AQPs was never or poorly regulated whatever the wideness of their expression domain and their expression level. Our work highlighted that PtTIP1;4 was the most responsive gene of the AQP family. A high functional divergence between gene duplicates was detected across species and in response to tested cues, except for the root-expressed PtTIP2;3/PtTIP2;4 pair exhibiting 80% convergent responses. Our meta-analysis assessed key features of aquaporin expression which had remained hidden in single experiments, such as expression wideness, response specificity and genotype and environment interactions. By consolidating expression profiles using independent experimental series, we showed that the large expansion of AQP family in poplar was accompanied with a strong divergence of gene expression, even if some cases of functional redundancy could be suspected.

The build-up of osmotic stress responses within the growing root apex using kinematics and RNA-sequencing

“…Osmotic stress also elicited expression of aquaporin , PtPIP2;7 , PtPIP2;10 , PtTIP1;1 , PtTIP1;2 , PtTIP2;2 , PtTIP2;3 , and PtTIP2;4 (Supplementary Table S4). Although members of this multigene family show redundancy and high stress responsiveness (Cohen et al , 2013), these transcriptional regulations suggested an increase in membrane hydraulic conductivity (Maurel, 2007). As cell expansion rate depends on wall extensibility as well as on membrane hydraulic conductivity (Lockhart, 1965), the up-regulation of aquaporin also pointed to facilitation of cell expansion.…”

The Eucalyptus Tonoplast Intrinsic Protein (TIP) Gene Subfamily: Genomic Organization, Structural Features, and Expression Profiles

“…This fact also suggests that certain isoforms might have acquired specific organ/tissue roles. Evidence from poplar trees, however, indicate that, in spite of their elevated tissue-specificity, a high level of functional redundancy exists amongst PtTIP members (Cohen et al, 2013). In this respect, the existence of functional redundancy between TIP genes was postulated in previous studies employing insertional Arabidopsis mutants (Schüssler et al, 2008).…”

“…In trees, the modulation of TIP expression in response to abiotic stress has been documented (Cohen et al, 2013; Rodrigues et al, 2013; Martins et al, 2015; Regon et al, 2014), and the major evidences point to a role for these proteins in stress adaptation. It is noteworthy that most of the EgTIP genes analyzed here displayed osmotic stress-responsive transcriptional profiles in three different organs.…”

Genome-wide identification and characterization of aquaporin gene family in common bean (Phaseolus vulgaris L.)

“…This differential expression could be plant-, aquaporin-, or stress-specific. Differential expression of aquaporins in response to different environmental stresses has been comprehensively evaluated in several plant species such as Arabidopsis, maize, poplar and B. rapa in the past years (Alexandersson et al 2005;Zhu et al 2005;Cohen et al 2013;Tao et al 2014). Regarding common bean, few aquaporins have been characterized to date.…”