How will rising atmospheric carbon dioxide concentrations affect phosphorus uptake in crops?

Take home messages

• Elevated atmospheric carbon dioxide (CO₂) concentrations can increase crop growth when sufficient phosphorus (P) is supplied.
• Crop are better able to acquire non-labile P under elevated CO₂ through increased root length in wheat and enhanced phosphatase activity in white lupin.
• High P-fixing soils may need increased P inputs so that the crops grown on these soils realise their increased crop yield potentials induced by elevated CO₂.

Background

Rising atmospheric CO₂ concentrations otherwise known as elevated CO₂, leads to an increase in C-fixation by crops. This elevated CO₂-induced increase in C-fixation leads to greater plant biomass and crop yields where nutrient supply is not limiting (Leakeyet al. 2009). With increased plant biomass and yields under elevated CO₂, it is anticipated that nutrient demand will increase, particularly for nitrogen (N) and phosphorus (P). There has been extensive work exploring the effects of elevated CO₂ on N dynamics in cropping systems but only limited work that looks at the effects on P dynamics (Lamet al. 2012; Jinet al. 2017). In highly weathered Australian soils that have high P-fixing capacity, P is one limiting plant nutrients in cropping systems and inputs of fertiliser P are an important driver of yield and profits (Kooymanet al. 2017).

Some crop species have adapted to acquire P from soils, despite its low availability to other species (Vuet al. 2010). Physiological adaptations are mechanisms which modify the rhizosphere environment and include exudation of organic acids and plant-derived phosphatases, and acidification. Morphological P acquisition traits involve increasing root length, altering root morphology and increasing the root-to-shoot ratio, enabling a greater soil volume to be exploited for P uptake. For example, wheat and faba bean have been shown to alter their root architecture in response to P deficiency, whereas species such as white lupin (Lupinus abus L.) upregulate exudation of organic acids and/or phosphatases to utilise non-labile P (Lyuet al. 2016). Elevated CO₂ can affect both physiological and morphological adaptation due to increased belowground C allocation and possibly increased P demand. For instance, it is widely known that elevated CO₂ enhances root length in a range of crop species, thus enabling crops to exploit a greater volume of soil. Furthermore, root exudation is also anticipated to increase as plants will have an excess of C that can be released as organic acids. The extent to which elevated CO₂ will increase a plant’s access to P under elevated CO₂ is unknown particularly in crop species with contrasting P acquisition strategies.

As elevated CO₂ generally increases crop yields, it is unknown if plants will require more available P in the soil to realise these yield increases. One method to determine the P demand of a crop species under elevated CO₂ is to apply increasing amounts of P to P-deficient soils. By generating a P response curve, the amount of P in the soil required to achieve maximum yield of a particular crop species can be determined. Furthermore, the present study examined if P or atmospheric CO₂ is limiting yield.

Method

Trial 1

Five crops (a wheat line without citrate exudation, a wheat line with citrate exudation, white lupin, faba bean and canola) were grown in a P-deficient Chromosol from Hamilton with a Bray-P of 5.1mg/kg. The two wheat lines were identical with the exception of a TaMATE1B gene, which confers a constitutive citric acid transporter (Hanet al. 2016). Crop species such as white lupin rely strongly on exudation of organic acids and phosphatases for P acquisition whereas faba bean displays a balance between physiological and morphological P adaptations. Plants were grown inside CO₂-controlled growth chambers under 20°C/16h days and 18°C/8h nights. The ambient and elevated CO₂ concentrations were 400ppm and 800ppm, respectively. Seventy days after sowing plant shoots were harvested and roots were removed from the soil. Rhizosphere soil was collected for phosphatase analysis.

Trial 2

This trial aimed to generate a P response curve for wheat. The plants were grown in two soils that contrasted in their P-fixing capacity. The high P-fixing soil was a Ferrosol and the low P-fixing soil was a Sodosol. The Ferrosol and Sodosol had P buffer index of 1095mg P/kg and 76mg P/kg, respectively and were both limed to a pH of 6. After addition of basal nutrients, increasing P rates were applied to each soil based on a previous incubation study (data not shown). The soil was transferred to columns (10cm x 30cm) with each containing 3kg of air-dry soil. The soils were pre-incubated for seven days and pre-germinated wheat seeds (Triticum aestivum L. cv. Yitpi^A) were sown. Growing conditions were identical to Trial 1. After five weeks, shoots and roots were harvested, and bulk soil was collected.

Measurements

Shoots and roots were oven dried at 70°C for two days then ground and digested in nitric-perchloric acid. The P concentration in the digests was determined using malachite green or ICP-OES.

Statistical analysis

A two-way analysis of variance (ANOVA) was performed using GENSTAT (version 19; VSN International, Hemel Hempstead, UK) to compare different treatments and their interactions. Differences between means were determined using the least significant differences (LSD).

Results and discussion

Elevated CO₂ enhanced total P uptake in canola and white lupin, but decreased P uptake in wheat without citrate exudation (by 18%) and faba bean (29%). It did not affect the P concentration in the shoot of citrate-exuding wheat, but decreased P concentration by 21% in non-citrate exuding wheat line (Table 1). The increase in P uptake in white lupin under elevated CO₂ may be explained through enhanced root exudation and increased phosphatase production which increased access to non-labile P sources. As elevated CO₂ can increase C fixation through photosynthesis, there may be more carbohydrates transferred below-ground and more organic acids (such as citric and malic acid) exuded from the root. The importance of organic acid exudation is outlined in the wheat lines where a lack of citric acid exudation led to a decrease in P uptake under elevated CO₂, whereas the wheat genotype that possessed the TaMATE1B gene was able to sustain P uptake under elevated CO₂. Furthermore, as elevated CO₂ increases P demand and uptake, up-regulation of phosphatase activity can also occur, leading to mineralisation of organic P in soil (data not shown).

Table 1. Shoot dry weight, P concentration and P uptake of wheat without citrate exudation (wheat –citrate), wheat with citrate exudation (wheat +citrate), white lupin, faba bean and canola grown for 70 days under ambient (A) and elevated (E) CO₂.

Elevated CO₂ did not affect shoot dry weight across all crop species in Trial 1 which could be due to low soil P availability limiting the promotion of plant growth under elevated CO₂. This is confirmed by the data in Table 2 where elevated CO₂ did not significantly increase the shoot dry weight of wheat at very low P rates. Results therefore suggest that crop yields will not benefit from elevated CO₂ in soils with low P availability. These results are supported by Jinet al. (2012) who showed no increase in soils without P addition.

Table 2. Shoot dry weight, P concentration and P uptake of wheat grown in a Ferrosol or a Sodosol with increasing P application rates. Plants were grown for 35 days either under ambient (A) or elevated (E) CO₂.

Through regression analysis, maximum shoot yield in Trial 2 was calculated to occur at 260mg P/kg and 350mg P/kg soil in the Ferrosol for ambient and elevated CO₂, respectively. This indicates that P supply may need to increase to benefit from the increased yields induced by elevated CO₂. In the Sodosol, the calculated P rate at which maximum shoot yield occurred was similar between ambient and elevated CO₂, occurring at around 280mg P/kg. Elevated CO₂ significantly increased the shoot yield by 28% in the Sodosol when P supply was at marginally deficient and adequate levels. This was associated with increased in root length and P uptake under elevated CO₂ (data not shown). The contrasting result between the Ferrosol and Sodosol is not clear but could be related to the diffusive supply of P (Mason et al. 2013) as the Sodosol may have some physical constraints. Given this, methods such as diffusive gradient in thin films (DGT) would be advantageous in estimating plant available P when compared to the conventional extraction methods used in this experiment.

Conclusion

Elevated CO₂ enhances P uptake in a P-deficient soil when the crop species grown are those that rely on organic acid exudation and phosphatase production. Furthermore, increased root length exhibited under elevated CO₂ aids in P acquisition and further enhances P uptake, particularly in low P-fixing soils.

Elevated CO₂ increased P requirements for the maximum biomass production of wheat plants grown in high P-fixing soils but not of those grown in low P-fixing soils.

References

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Mason, SD, McLaughlin, MJ, Johnston, C, McNeill, A (2013) Soil test measures of available P (Colwell, resin and DGT) compared with plant P uptake using isotope dilution. Plant and Soil 373, 711-722.

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Acknowledgements

The authors thank Mark Richards from NSW Department of Primary Industries for supplying the white lupin seeds and Dr Manny Delhaize from CSIRO for providing the wheat seeds. James O’Sullivan is supported by the Australian Government Research Training Program.

Contact details

James B O’Sullivan
La Trobe University, AgriBio Centre for AgriBiosciences, Bundoora, VIC 3086
jbosullivan@students.latrobe.edu.au
@JamesOSoilivan