CO2 elevation modulates the response of leaf gas exchange to progressive soil drying in tomato plants

doi:10.1016/j.agrformet.2019.01.026

Agricultural and Forest Meteorology

Volume 268, 15 April 2019, Pages 181-188

https://doi.org/10.1016/j.agrformet.2019.01.026 Get rights and content

Highlights

•
The modulation of elevated CO₂ on stomatal response to progressive drought was studied in tomato plants.
•
Elevated CO₂ retarded the response of photosynthesis and stomatal conductance to soil water deficits.
•
The responsiveness of stomatal conductance to ABA was unaffected by CO₂ environment.
•
Elevated CO₂ enhanced both water use efficiency and nitrogen use efficiency in tomato plants.

Abstract

The objective of this study was to investigate the response of leaf gas exchange of tomato plant to progressive drought stress under ambient (a[CO₂], 400 ppm) and elevated (e[CO₂], 800 ppm) atmospheric CO₂ concentration. The fraction of transpirable soil water (FTSW) was used to evaluate soil water status in the pots. The results showed that stomatal conductance (g_s) and transpiration rate (T_r) were significantly lower while the net photosynthetic rate (A_n) was significantly higher in plants grown under e[CO₂] than those under a[CO₂] at onset of drought stress. Along with soil drying, the FTSW thresholds at which g_s and A_n started to decrease were significantly lower in plants grown under e[CO₂] as compared to plants grown under a[CO₂]. The intrinsic water use efficiency and instantaneous water use efficiency of plants grown under e[CO₂] was significantly higher than those under a[CO₂]. Under e[CO₂], the drought-stressed plants had greater leaf area, dry matter and water use efficiency than those grown under a[CO₂]. e[CO₂] notably enhanced shoot C concentration while decreased shoot N concentration hereby increased the C:N ratio. With the decrease of FTSW, the concentration of abscisic acid in leaf ([ABA]_leaf) and xylem sap ([ABA]_xylem) increased exponentially. When FTSW > 0.2, under both CO₂ environments, g_s decreased linearly with increasing [ABA]_leaf and [ABA]_xylem; and similar slopes but different intercepts were noticed for the regression lines, indicating that the responsiveness of g_s to ABA was unaffected by CO₂. In conclusion, CO₂ elevation retarded the response of leaf gas exchange to progressive soil drying in tomato plants. This result provides novel knowledge for more precise prediction of plant response to drought stress in a future CO₂-enriched environment.

Introduction

Currently, the atmospheric CO₂ concentration ([CO₂]) has exceeded 400 ppm (Tans and Keeling, 2018) and is expected to double at the end of this century (Intergovernmental Panel on Climate Change, 2013), mainly due to anthropogenic activities as fossil fuel burning and deforestation (Qaderi and Reid, 2009). The elevated CO₂ (e[CO₂]) is a potential driver for increasing global temperature and changing precipitation patterns, leading to drought at both regional and global level. Drought is one of the most important factors restricting crop production in many areas of the world (Boyer et al., 2013). Therefore, a better understanding of plant responses to rising CO₂ and drought is essential for enhancing crop yield and water use efficiency (WUE) in future climate.

Stomata are tiny openings in plant tissue that allow for gas exchange between plants and atmosphere. Stomatal aperture is regulated by various environmental factors, including atmospheric CO₂ concentration (Mansfield et al., 1990; Assmann, 1999; Azoulay-Shemer et al., 2015), leaf to air vapour pressure deficit (VPD) (Yong et al., 1997; Bunce, 1998; Li and Li, 2014), and water status of the plant (Liu et al., 2005). In relation to plants grown at ambient CO₂ concentration, stomata tended to open at low CO₂ level but tended to close at e[CO₂] (Lee et al., 2008; Merilo et al., 2014). During progressive soil drying, plants can sense the water availability around the roots and respond by sending chemical signals (mainly xylem-borne abscisic acid, [ABA]_xylem) to the shoot, narrowing stomatal apertures, thus decrease stomatal conductance (g_s) (Zhang and Davies, 1990; Liu et al., 2005). Nevertheless, recent study by Zhang et al. (2018) showed that rapid ABA biosynthesis predominantly occurs in the leaves, and not in other tissues in angiosperms following a short-term reduction in cell volume generated by the application of external pressure. It is widely accepted that, both e[CO₂] and soil water deficit could reduce g_s (Xu et al., 2016; Yan et al., 2017), and soil water deficit has a stronger influence on g_s than e[CO₂] when combined factors exposed (Leakey et al., 2006). Some researchers suggested that e[CO₂] could relieve drought damage by reducing g_s and transpiration rate (T_r) to sustain a high leaf water potential (Tardieu and Simonneau, 1998; Tausz-Posch et al., 2015). However, recent study revealed that g_s of plant leaves under e[CO₂] decreased later but more sharply than that under a[CO₂] during progressive soil drying (Yan et al., 2017). Moreover, Yan et al. (2017) found that at a[CO₂] the decrease of g_s in tomato leaves was mainly regulated by the [ABA]_xylem at moderate drought stress; while under e[CO₂] the g_s was predominately controlled by leaf turgor pressure. While, there was no information related to leaf ABA ([ABA]_leaf), which may also involve in regulating g_s of tomato plants subjected to drought in different CO₂ environments. In addition, whether e[CO₂] could modulate the response of g_s to water deficits remains largely elusive, and the mechanisms by which g_s is regulated under combined drought and e[CO₂] are still need to be investigated.

It is well recognized that plants grown at e[CO₂] had increased leaf photosynthetic rate (A_n), decreased g_s and T_r, thus resulting in improved WUE at stomatal and leaf scales (Drake et al., 1997; Kang et al., 2002; Yan et al., 2017; Wei et al., 2018). Furthermore, the increased A_n lowered T_r of plants grown under e[CO₂] often associated with greater biomass and reduced water consumption resulting in an improved WUE at plant level (Pazzagli et al., 2016). On the other hand, plant N could regulate C metabolism in plants, as N is an essential component for all of the enzymes involving in carbohydrate metabolism, transport and utilization (Huppe and Turpin, 1994). Moreover, mineral concentrations especially N concentration ([N]) in plants grown at e[CO₂] was often found to decrease, mostly due to the dilution effect by the increased biomass and reduced root N uptake resulting from limited transpiration mass flow of plant (Taub and Wang, 2008; Myers et al., 2014). It is worth noting that at a reduced N nutrition, e[CO₂] increased cytokinins delivery to the leaf causing stomatal opening (Yong et al., 2000; Teng et al., 2006), which may offset the effect of ABA-induced stomatal closure under moderate drought. It has been reported that carbon and nitrogen ratio ([C:N]) in plant dry biomass could indicate the amount of carbon fixed per unit N acquired, and could be used as an indicator of nitrogen use efficiency (NUE) (Livingston et al., 1999; Wang et al., 2010; Wei et al., 2018). An increased NUE has frequently be observed from plants grown at e[CO₂] (Reddy et al., 2010). However, the mechanism by which NUE is modified remains unknown when plants exposed to combined drought stress and e[CO₂] environment.

Therefore, the objective of the present study was to investigate the effects of e[CO₂] as compared with a[CO₂] on the response of leaf gas exchange, plant water relations and plant growth in tomato plants to progressive soil drying. Tomato plants were transplanted in two atmospheric [CO₂] (400 and 800 ppm) environments at 4-leaf stage. Eleven days after transplanting in each cell, 4 plants were well watered and others (20 plants) were exposed to progressive drought stress by withholding irrigation lasting 8 days. Leaf gas exchange, plant water relations, shoot dry mass, WUE in stomatal, leaf and plant scopes, leaf area, concentrations of [C] and [N] in leave and stem, and ABA concentration in leaf and xylem sap were measured. It was hypothesized that: 1) [ABA]_leaf and [ABA]_xylem would be involved in regulation of g_s during drought stress in both a[CO₂] and e[CO₂] environments; and 2) due to the initial lower g_s of plants grown under e[CO₂], it would retard the decline of g_s during the soil drying.

Section snippets

Experimental setup

Pot experiment was conducted in climate-controlled greenhouses at Faculty of Science, University of Copenhagen, Taastrup, Denmark. Tomato seeds were sown on 14th December 2017. At the 4-leaf stage, seedlings were transplanted to 3 l pots filled with 0.9 kg peat (Pindstrup substrate no. 2, Pindstrup Mosebrug A/S, Pindstrup, Denmark) in greenhouse cells with CO₂ concentration of 400 ppm (ambient CO₂, a[CO₂]) and 800 ppm (elevated CO₂, e[CO₂]). The [CO₂] was sustained by pure CO₂ emission from a

Leaf gas exchange

At onset of drought stress, plants grown under e[CO₂] had notably 34.8% lower stomatal conductance (g_s) than those grown under a[CO₂] (Fig. 3a; Table 1). Along with the progressive soil drying, g_s of the plants grown under e[CO₂] began to decline linearly when FTSW decreased to 0.40, which was significantly lower than those grown under a[CO₂], i.e., 0.61 (Fig. 3a; Table 1). Upon onset of drought stress, the net photosynthetic rate (A_n) in plants grown under e[CO₂] was 24.5% higher than those

Discussion

Under non-drought stress conditions, the g_s in plants grown at e[CO₂] was significantly lower compared to those grown at a[CO₂] (Fig. 3a), in accordance with the early findings that e[CO₂] induced stomatal closure thus lowering g_s (Kang et al., 2002; Azoulay-Shemer et al., 2015; Easlon et al., 2015). The signals inducing stomatal closure under e[CO₂] are still elusive, and both ABA-dependent and independent pathway could exist (Hus et al., 2018). Early study by Raschke (1975) illustrated that

Conclusion

Conclusively, plants grown under e[CO₂] delayed A_n and g_s response to progressive soil drying. The mechanism by which decreases of g_s in plants under a[CO₂] could be regulated by both [ABA]_leaf and [ABA]_xylem, while under e[CO₂] at moderate drought could be ABA-independent. e[CO₂] did not influence plant water relations in the well-watered plants and drought plants which most probably due to higher VPD under e[CO₂]. Additionally, e[CO₂] decreased [N]_shoot and enhanced [C:N]_leaf both in

Acknowledgements

Jie Liu appreciate the Chinese Scholarship Council (CSC) for supporting his study at the Faculty of Science, University of Copenhagen, Denmark. Technical assistance by René Hvidberg Petersen and Lene Kofsholm Jørgensen is gratefully acknowledged.

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Citation Excerpt :
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Earlier studies have recommended 0.5–0.8 kPa of VPD was suitable for tomato cultivation in greenhouse (Bakker, 1990) as too high or too low VPD can induce suppression of gs for CO2 diffusion (Dorais et al., 2004) or leaf physiological disorders (Bertin et al., 2000; Holder and Cockshull, 1990). It is well known that plant gs was determined by stomata density and aperture, which were closely related to growth environment and plant hormones (Yong et al., 1997; Liu et al., 2019). Literatures documented that gs decreased in response to higher VPD (Du et al., 2020; Maroco et al., 1997; Yong et al., 1997) to reduce evapotranspiration.
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CO2 elevation modulates the response of leaf gas exchange to progressive soil drying in tomato plants

Highlights

Abstract

Introduction

Section snippets

Experimental setup

Leaf gas exchange

Discussion

Conclusion

Acknowledgements

Global Food Secur.

Environ. Exp. Bot.

Trends Ecol. Evol.

Agric. Water Manage.

Trends Plant Sci.

Eur. J. Agron.

Agric. Water Manage.

Agric. Water Manage.

Enviro. Exp. Bot.

Determination of Abscisic Acid by Indirect Enzyme Linked Immuno Sorbent Assay (ELISA)

The cellular basis of guard cell sensing of rising CO2

Plant Cell Environ.

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Plant J.

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J. Biogeogr.

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Annu. Rev. Plant Physiol. Plant Mol. Biol.

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Benefits of CO2 enrichment on crop plants are modified by soil water status

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Plant Physiol.

CO₂ elevation modulates the response of leaf gas exchange to progressive soil drying in tomato plants

The cellular basis of guard cell sensing of rising CO₂

Guard cell photosynthesis is critical for stomatal turgor production, yet does not directly mediate CO₂ - and ABA- induced stomatal closing

More efficient plants: a consequence of rising atmospheric CO₂?

Does low stomatal conductance or photosynthetic capacity enhance growth at elevated CO₂ in Arabidopsis?

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Benefits of CO₂ enrichment on crop plants are modified by soil water status