Research article
The root cortex cell hydraulic conductivity is enhanced with increasing chromosome ploidy in wheat

https://doi.org/10.1016/j.plaphy.2013.03.021Get rights and content

Highlights

  • The root hydraulics and TaPIPs transcription of polyploid wheat roots were studied.

  • The cortex cell hydraulic conductivity increased with increasing ploidy.

  • TaPIP1;2 and TaPIP2;5 transcription increased with increasing ploidy.

  • Results provide insight into the enhanced root water uptake during wheat evolution.

Abstract

Wheat (Triticum spp.) root water uptake is enhanced with increasing chromosome ploidy, but the underlying mechanism is unclear. The leaf transpiration rate (E), individual root (Lpr) and cortical cell (Lpc) hydraulic conductivity, cortical cell volume (Vc) and transcription levels of two putative plasma intrinsic aquaporin genes (PIPs) were investigated in wheat seedlings with different chromosome ploidy (Triticum monococcum (2X, AA); Triticum dicoccum (4X, BB); Triticum aestivum (6X, AABBDD)). The E, Lpr and Lpc of wheat increased with increasing ploidy, but the Vc was reduced. Osmotic stress significantly reduced the E, Lpc, Lpr, and the relative mRNA content of TaPIP1;2 and TaPIP2;5 in wheat. Under both well-watered and osmotic stress conditions, the Lpr was significantly and positively correlated with the E and Lpc, and the relative mRNA content of TaPIP1;2 and TaPIP2;5 was significantly and positively correlated with Lpc and Lpr, respectively. For well-watered or osmotically stressed wheat plants, the Lpc was reduced, but the Lpc/Lpr increased with increasing Vc, suggesting that Vc affects root radical water transport. Thus, the increased Lpc and transcription levels of TaPIP1;2 and TaPIP2;5 in wheat roots provides insight into the mechanisms underlying enhanced root water uptake with increasing chromosome ploidy during wheat evolution.

Graphical abstract

The cortex cell hydraulic conductivity (Lpc) in wheat roots increases with increasing chromosome ploidy. The relative mRNA content of TaPIP1;2 and TaPIP2;5 was also significantly increased and positively correlated with the Lpc and Lpr. These results might provide insight into the mechanism underlying enhanced root water uptake with ploidy increase during wheat evolution.

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Introduction

Plant growth depends on an optimum balance between water uptake in the roots and water losses through the shoots. In the past decades, the physiological and morphological responses of crops to soil water shortage have been studied to reduce shoot transpiration [1], [2], and deficit irrigation has been an important approach to reduce water use and improve water use efficiency in agriculture [3], [4]. However, the roots typically provide the water input in whole-plant water balance and, hence, play a central role in maintaining the plant water status in a changing water environment [5]. Due to technical problems, the basic hydraulic properties of roots are not yet adequately understood [6]. Based on the results obtained from early anatomical and experimental studies using root and cell pressure probes, a composite model of water transport in roots was proposed [7]. The model postulates that water moves across plant tissues through both apoplastic and cell-to-cell pathways. The cell-to-cell pathway refers to water flow through the plasmodesmata and/or across membranes, substantially contributing to whole-plant hydraulic resistance [8]. Peter Agre et al. identified aquaporins (AQPs), which substantially changed the understanding of the water trans-membrane movement mechanism [9] and provided a molecular basis for plant water transport and regulation.

AQPs are biological membrane structures belonging to the major intrinsic protein (MIP) superfamily [10]. AQPs have been divided into four or five subfamilies, and the plasma membrane intrinsic proteins (PIPs) are primarily located in the plasma membrane [11], [12]. PIPs can be further subdivided into PIP1 and PIP2 groups [13]. In contrast with PIP1 proteins, the overexpression of PIP2 proteins considerably increased the water permeability of oocyte membranes [14], [15]. However, the coexpression of PIP1;2 and some PIP2 isoforms further increased the water permeability of oocyte membranes [16], indicating the roles of PIP proteins in regulating water permeability through the formation of heterologous tetramers. Studies have implicated a role for PIPs in regulating leaf and root hydraulic properties. PIPs have been isolated from cells in the root cortex, root endodermis, leaf xylem parenchyma and bundle sheath in plants [17], [18]. PIP1 or PIP2 antisense lines exhibited reduced root hydraulic properties and recovered more slowly after rewatering than wild-type lines [19], [20]. Diurnal variations in the root hydraulic conductivity of Lotus japonicus and maize (Zea mays L.) have been associated with the expression of some aquaporins, particularly PIP2 [21], [22]. However, in grapevine (Vitis vinifera), the increased expression of PIP1;1 reflected diurnal variation in the root system and cortical cell hydraulic conductivity (Lpc) in response to water stress, while the expression of PIP2;2 did not change [23]. Furthermore, PIP1;2 and PIP2;5 have been associated with cell membrane and/or root hydraulic conductivity in Oryza sativa [24], Arabidopsis [25], and maize [26]. Zhang and Tyerman [27] reported that HgCl2 largely inhibited the Lpc of wheat, which suggests a role for aquaporins in cortex cell hydraulics. TaPIP1;2 and TaPIP2;5 have been identified in wheat, and the sequences of these genes have been submitted to the NCBI sequence database [28]. However, there are few studies concerning the relationships between TaPIP1;2 and TaPIP2;5 and root hydraulic traits in wheat (Triticum spp.).

Many cereal grasses, such as wheat, have complex genomes with several genotypes: diploid, tetraploid and hexaploid species. Wheat has been cultivated for over 10,000 years and has become one of the most important cereal crops worldwide [29]. In China, wheat accounts for 22–27% of total crop sown area in the past decade [30]. Thus, characterizing the photosynthetic features and water use efficiency of wheat has garnered much attention in scientific research [31], [32], [33]; however, root water uptake in wheat has received much less attention. Zhao et al. showed that the root system (Lprs) and individual root (Lpr) hydraulic conductivity increased with increasing chromosome ploidy (2X → 6X) [34], thereby enhancing root water uptake with increased ploidy. However, changes in the Lpc of wheat with increased ploidy have not been reported.

We hypothesize that the Lpc of wheat increases with increasing ploidy, and the expression of TaPIP1;2 and TaPIP2;5 is associated with root hydraulic traits. To confirm this hypothesis, we selected three wheat cultivars with differing ploidy classes (Triticum monococcum (M; 2X); Triticum dicoccum (D; 4X); Triticum aestivum (A; 6X)) based on our former research [34]. The Lpr, Lpc and expression of TaPIP1;2 and TaPIP2;5 transcripts in wheat seedlings under two water supply conditions were examined. In this study, we reveal the relationships between Lpr, Lpc, gene transcription, cortex cell volume and leaf water status in wheat plants.

Section snippets

Leaf gas exchange in different ploidy classes of wheat

For well-watered plants, the leaf transpiration rate (E) and stomatal conductance (gs) ranged from 1.57 to 2.74 mmol m−2 s−1 and 80 to 160 mmol m−2 s−1, respectively (Fig. 1A and B). The E and gs of well-watered plants increased with increasing chromosome ploidy. The osmotic stress induced with 10% PEG6000 significantly reduced the E (40%) and gs (30%) in the three wheat cultivars, except for the E of T. dicoccum, which was not significantly different from that of well-watered and osmotically

Discussion

Clarifying the mechanisms underlying root water uptake is important to understand whole-plant water balance and improve water use efficiency in wheat. Using wheat plants with different ploidy levels, we investigated leaf transpiration, individual root and cortex cell hydraulic conductivities and the transcription levels of TaPIP1;2 and TaPIP2;5. Based on these results and the data obtained from previous studies, some questions and hypotheses concerning root water uptake will be discussed.

Conclusion

Using wheat plants with different ploidy levels, we showed that leaf transpiration, individual root and cortical cell hydraulic conductivities and the transcription levels of TaPIP1;2 and TaPIP2;5 increased with increasing ploidy. The Lpc was significantly correlated with the Lpr, and the cortical cell volume might affect the contribution of the cell-to-cell pathway in root radical water transport. The transcription levels of TaPIP1;2 and TaPIP2;5 were correlated with Lpc and Lpr. Taken

Plant material and treatments

The wheat seeds (T. monococcum (2X, AA); T. dicoccum (4X, AABB); T. aestivum (6X; cv: Shaan253, AABBDD)) were disinfected using 2% sodium hypochlorite, rinsed with distilled water, and placed on moist filter paper for 2 days at 25 °C in a dark chamber for germinating. The seedlings were raised hydroponically in a growth chamber under a 12/12 h photoperiod (25/18 °C; RH 50−60%; 400 μmol photons m−2 s−1). Half-strength modified Hoagland's nutrient solution (pH 6.0) was used for well-watered plants

Acknowledgments

This study was supported through funding from the National Basic Research Program of China (2009CB118604), the National Natural Science Foundation of China (30971714), and the 111 project of Chinese Education Ministry (B12007).

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    Weifeng Wang and Xiaoqing Yang are co-first authors who contributed equally to this work.

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