Elsevier

Journal of Proteomics

Volume 74, Issue 8, 12 August 2011, Pages 1396-1410
Journal of Proteomics

Poplar under drought: Comparison of leaf and cambial proteomic responses

https://doi.org/10.1016/j.jprot.2011.03.013Get rights and content

Abstract

The forest ecosystem is of particular importance from an economic and ecological perspective. However, the stress physiology of trees, perennial and woody plants, is far from being fully understood. For that purpose, poplar plants were exposed to drought; the plants exhibited commonly reported drought stress traits in the different plant tissues.

Leafy rooted cuttings of poplar were investigated through a proteomic approach in order to compare the water constraint response of two plant tissues, namely leaf and cambium. Sampling was realized during the drought period at 2 time points with increased drought intensity and 7 days after rewatering.

Our data show that there is a difference in the moment of response to the water constraint between the two tissues, cambium being affected later than leaves. In leaves, drought induced a decrease in rubisco content, and an increase in the abundance of light harvesting complex proteins as well as changes in membrane-related proteins. In the cambial tissue, the salient proteome pattern change was the decrease of multiple proteins identified as bark storage proteins. After rewatering, almost all changes in cambial proteome disappeared whereas a significant number of leaf proteins appeared to be differentially regulated only during the recovery from drought.

Graphical abstract

Poplar plants exposed to drought exhibit contrasting proteomic response in leaf and cambium. Seven days after rewatering leaf proteome remained altered while cambial proteome showed few differences compared to control.

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Introduction

Water deficit represents the most recurrent and the most serious environmental drawback for plants [1]. Considering the worldwide increasing frequency of extreme weather events forecasted by climate modeling [2], intensive efforts are made to appreciate plant adjustment abilities to environmental stresses, especially drought [3].

The forest ecosystem is of particular importance from an economic, biological, atmospheric and hydrological perspective. At the regional scale, CO2 and water vapor exchanges between woody species and air have been demonstrated to influence the climate [4]. As harsher climate conditions threaten forest health, distribution and composition [5], it becomes important to decipher the stress-coping mechanisms implied in stress tolerance of trees.

Among trees under temperate latitude, Populus species exhibit the greatest growth rates at the expense of large water requirements [6]. Although species and cultivars present a wide genetic variability in traits related to water deficit tolerance whatever the age or the environment of the plant (greenhouse, nursery, or plantation) [7], [8], [9], poplar plants are known to be among the most sensitive woody plants to water stress [10] with cavitation events beginning as soon as xylem tension reaches the range of − 1 to − 1.5 MPa. This is the reason why the samples used for the proteomic study where collected when the predawn leaf water potential reached − 0.5 MPa and − 0.9 MPa.

Poplar whose genome was recently fully sequenced [11] has become a model plant for molecular studies in forestry. Its study brings insights into phenomena specific to trees such as wood formation or seasonality. Its range of reactions to biotic and abiotic factors is widely considered in the literature, especially at leaf [12], [13], root [14], [15] and xylem [16] levels. Hence, the use of poplar enables not only to understand specific aspects of the tree's response to each type of stress in each kind of tissue, but also the common features of the plant cell exposed to a stressing condition. Moreover, to sustain the extension of poplar cultivation from flood plains and bottomlands to uplands where soil water availability is subjected to seasonal changes, more water-use-efficient and drought tolerant hybrids are required. It is also noteworthy that over the last decades, episodes of dry weather (sometimes followed by short flooding events) have been observed in regions where poplars are cultivated or naturally distributed.

Poplar drought stress responses at the root level [17], the leaf level [18], or both [19] have been extensively documented. Given that these organs are responsible for the water dynamics inside the whole plant, they must react rapidly to a stress in order to allow plant survival. On the long run, a successful reaction should result in acclimation, which requires that each part of the organism fine-tunes to suboptimal conditions. The perception of the constraint largely depends upon the position, the age and physiological stage of the organ [20], [21]. Among the tree tissues, some further investigation is needed to unravel the cambium response to stress, as this specific tissue is responsible for perennial life of trees through secondary growth and wood formation, an exclusive histological trait of woody plant species [22]. Knowing the functioning of cambium during drought stress is critical for an integrative comprehension of the plant response which relies on multiple and complex processes. Cambium during water deficit has been studied in a few articles [12], [23], but seldom within a proteomic approach [19].

Since gene transcription level is not automatically correlated to the actual abundance of active proteins, and given that the poplar genome, although sequenced, is not fully annotated yet, untargeted approaches such as proteomic studies keep on constituting effective tools for the identification and for time-dynamics assessment of biological functions affected by a constraint.

The present research paper aims at characterizing the physiological state of poplar plants at 2 time points of a gradually imposed water constraint, mild and severe stress, and after a recovery period. A quantitative proteomic analysis was undertaken for the identification of proteome changes in leaf and cambium in response to the constraint. The hybrid poplar genotype INRA 717-1B4 was chosen because of its rapid growth and its use as a forest model species [24]. The other reason is that this genotype can be genetically transformed with Agrobacterium and regenerated efficiently into transgenic trees within 6–10 months [25]. Thus it will be easy in the future to use transgenic plants from this genotype to demonstrate protein function.

Section snippets

Plant material and water constraint

Rooted cuttings of Populus tremula L. × P. alba L. (Populus × canescens (Aiton) Smith) genotype INRA 717-1B4 were placed in 10 dm3 pots filled with a sand–peat moss soil mixture (25:75, v/v, pH 6.9) in a growth chamber. Control conditions were set at 22 °C, 70% relative humidity, and irradiance of 1000 μmol m 2 s 1 provided during 16 h per day. The branches collected from the nursery and used to obtain the rooted cuttings were divided in 15 cm length cuttings made up of two or three buds. During the

Physiological results

The predawn leaf water potential (Ψ) of control plants was equal to − 0.2 MPa throughout the experiment (Fig. 1). Withholding water induced a significant decrease in Ψ from day 6 on. At day 8 and 12 Ψ of stressed plants reached − 0.5 MPa, and − 0.9 MPa respectively. Four days after rewatering, Ψ returned to control values, − 0.2 MPa.

The stem water content of control plants oscillated during the experiment between 54.8 and 56.2% (Table 1). Withholding water did not significantly modify this parameter

Physiological status

As a first reaction to water deficit, plants generally tend to close their stomata, a reaction especially noted in poplar [35], [36]. The main goal of stomatal closure is to limit water losses and subsequent tissue damage; the irreversible cavitation of xylem is avoided in particular, although stomatal closure also induces a putative shortage in energy supply that can affect the whole metabolism in the mid- to long-term [37].

In the present study, the water starvation resulted in a significant

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