Introduction

Plants have evolved a range of adaptions for optimizing acquisition of mineral nutrients. Thus, plants experiencing low-nitrogen (N) availability are characterized by a high-root mass fraction, increased root branching and increased root surface area through an extensive production of root hairs, and in relevant cases, symbiotic interactions with mycorrhizal fungi. These features of N-starved plants are well known from both old (Brouwer, 1962; Ågren & Ingestad, 1987) and more recent (Hermans et al., 2006) studies and molecular cues underpinning such plant responses have been described (Kiba & Krapp, 2016). Based on data from 77 studies and 129 species, Reynolds & D'Antonio (1996) observed that in the majority of the cases, the root biomass ratio increased with decreased nitrogen availability. It has been assumed that such phenotypic characteristics will increase the fitness of plants in low-N environments through enhancing the ability to acquire the limiting resource – N (Brouwer, 1962). An increase in root hair density and/or -length is reported in a range of studies for nutrients that are relatively immobile in soil such as phosphorus and potassium (Gahoonia et al., 1997; Gahoonia & Nielsen, 1998; Bates & Lynch, 2001; Jungk, 2001; Bienert et al., 2021), but also for nutrients with higher mobility like inorganic N when occurring at low concentrations (Bhat et al., 1979; Foehse & Jungk, 1983; Ewens & Leigh, 1985; Saengwilai et al., 2021).

Plant N acquisition is mainly governed by two processes: diffusion (movement of N molecules through the soil water driven by a concentration gradient) and mass flow (transport together with soil water) (Nye, 1977; Tinker & Nye, 2000; McMurtrie & Näsholm, 2018). With decreasing N supply rates, concentrations of N in the soil solution decreases and hence the relative contribution of mass flow decreases. Consequently, plant responses to low-N supply should be aimed towards optimization for N acquisition via diffusion and this is mainly accomplished through an increase in root surface area. A model describing plant optimization for N acquisition (McMurtrie & Näsholm, 2018) points to the possibility that mass flow is enhanced when the internal spacing of roots (i.e. the mean distance between roots of the same plant) is large, and when the total root surface area is low. Thus, optimization of mass flow-driven N acquisition will predictably lead to lower N acquisition via diffusion. This suggests a trade-off between plant optimization for diffusive and mass flow-mediated N acquisition.

Plant acquisition of organic N should therefore primarily be governed by diffusion while acquisition of inorganic N, in particular, NO₃⁻, should be governed by mass flow.

From the above one may conclude that for both low-N supply and for a dominance of organic N, plant fitness is linked to characteristics that optimizes N acquisition via diffusion, and hence phenotypic shifts associated with low-N availability should overlap with those related to organic N nutrition.

In nonmycorrhizal plants, the abundance and length of root hairs are pivotal for the total root surface area (Jungk, 2001; Smith & De Smet, 2012). As discussed above, root hair growth is highly responsive to the supply of immobile nutrients such as phosphate and potassium. Following the same logic, we can infer that root hair growth should also be responsive to immobile N forms. Root and root hair proliferation are dependent on photosynthetically derived carbohydrates but the actual costs in terms of energy and carbon (C) is strongly dependent on the source of N acquired by roots. Thus the biochemical cost for assimilation of different N forms varies and is substantially higher for NO₃⁻ compared to NH₄⁺ (Bloom et al., 2003). The difference is even greater comparing NO₃⁻ and organic N such as the amino acids glutamine and arginine (Zerihun et al., 1998; Franklin et al., 2017). Here, the difference originates both from the lower energetic requirements for reduction and assimilation of N but also from the extra C derived from uptake of organic N. A model based on these differences in biochemical costs of assimilation predicts a significant increase in root mass fraction linked to organic N nutrition (Franklin et al., 2017). This would provide a feed-forward mechanism by which the lower costs for assimilation and the C bonus from organic N uptake enables a larger root surface investment that, in turn, enhances organic N nutrition.

Carbon use efficiency (CUE), the ratio of photosynthesis to respiration, is a critical factor for the global carbon budget and a key parameter in global vegetation models. It is well known that plant CUE is influenced by nutrient, in particular N, availability (Vicca et al., 2012) but to what extent plant use of organic or inorganic N may affect plant CUE has not been investigated. However, the above-described differences in C costs pertaining to uptake and assimilation of different N forms would theoretically also influence plant CUE. Analysing the potential impact of organic vs inorganic N nutrition on plant CUE may hence provide important information for the development of new global C models.

Here, we theoretically (through modelling) and experimentally analysed the expected effects of different N forms on plant growth and C and N allocation. We grew Arabidopsis thaliana (Arabidopsis) axenically to investigate how root : shoot allocation, root hair formation, and CUE compares between the two N sources NO₃⁻ and l-gln. We hypothesized that plants grown on the organic N source would display a reduced N uptake per root mass, increased root biomass and -surface area, and an increase in root mass fraction. We used stable isotope labelling (¹³C and ¹⁵N) to quantify uptake and distribution of N and C sources by plants, enabling assessment of the role of C uptake for the development of an organic N phenotype and enabling calculation of effects of organic N uptake on plant CUE.

中文翻译：

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植物有机氮营养：成本、收益和碳利用效率

 介绍

植物已经进化出一系列适应性，以优化矿物养分的获取。因此，低氮 （N） 可用性的植物的特点是根质量分数高，根分枝增加，根表面积增加，通过根毛的广泛生产，以及在相关情况下，与菌根真菌的共生相互作用。缺氮植物的这些特征在老（Brouwer，1962 年;Ågren和Ingestad，1987）和最近的（Hermans等 人，2006）的研究以及支撑这种植物反应的分子线索已经被描述过（Kiba & Krapp，2016）。 根据来自77项研究和129个物种的数据，Reynolds&D'Antonio（1996）观察到，在大多数情况下，根生物量比例随着氮可用性的降低而增加。据推测，这种表型特征将通过增强获取限制资源 – 氮的能力来提高植物在低氮环境中的适应性（Brouwer， 1962）。在一系列研究中报告了根毛密度和/或长度的增加，这些营养物质在土壤中相对不动，如磷和钾（Gahoonia et al.， 1997;Gahoonia & Nielsen， 1998;Bates & Lynch， 2001;Jungk，2001 年;Bienert等 人，2021 年），也适用于低浓度出现时具有较高迁移率的营养物质，如无机氮（Bhat 等 人，1979 年;Foehse & Jungk， 1983;Ewens & Leigh， 1985;Saengwilai等 人，2021 年）。

植物氮的获取主要由两个过程控制：扩散（氮分子在浓度梯度驱动的土壤水中的运动）和质量流（与土壤水一起运输）（Nye，1977 年;Tinker & Nye， 2000;McMurtrie & Näsholm，2018 年）。随着氮供应速率的降低，土壤溶液中氮的浓度降低，因此质量流量的相对贡献减小。因此，植物对低氮供应的反应应旨在优化通过扩散获取氮，这主要是通过增加根表面积来实现的。一个描述植物优化氮采集的模型（McMurtrie & Näsholm，2018 年）指出，当根的内部间距（即同一植物的根之间的平均距离）较大且总根表面积较低时，质量流量可能会增强。因此，可以预见，优化质量流驱动的氮采集将导致通过扩散降低氮采集。这表明在扩散和质量流介导的 N 采集的被控对象优化之间进行权衡。

因此，植物对有机氮的获取应主要由扩散控制，而无机氮的获取，特别是 NO₃⁻，应由质量流控制。

从以上可以得出结论，对于低氮供应和有机氮的优势，植物适应性与通过扩散优化氮获取的特性有关，因此与低氮可用性相关的表型变化应与有机氮营养相关的表型变化重叠。

在非菌根植物中，根毛的丰度和长度对于总根表面积至关重要（Jungk，2001 年;Smith & De Smet，2012 年）。如上所述，根毛的生长对磷酸盐和钾等固定营养物质的供应高度敏感。按照同样的逻辑，我们可以推断根毛的生长也应该对不动的 N 形式做出反应。根和根毛的增殖取决于光合作用衍生的碳水化合物，但能量和碳 （C） 的实际成本在很大程度上取决于根获得的氮来源。因此，不同 N 形式同化的生化成本各不相同，与 NH₄⁺ 相比，NO₃⁻ 的生化成本要高得多（Bloom et al.， 2003）。与 NO₃⁻ 和有机氮（如氨基酸谷氨酰胺和精氨酸）相比，差异更大（Zerihun 等 人，1998 年;Franklin等 人，2017 年）。在这里，差异既源于还原和同化 N 的较低能量需求，也源于有机 N 吸收产生的额外 C。基于同化生化成本这些差异的模型预测与有机氮营养相关的根质量分数显着增加（Franklin et al.， 2017）。这将提供一种前馈机制，通过该机制，较低的同化成本和有机氮吸收的碳奖励使更大的根表面投资成为可能，从而增强有机氮的营养。

碳利用效率 （CUE） 是光合作用与呼吸作用的比率，是全球碳收支的关键因素，也是全球植被模型中的关键参数。众所周知，植物 CUE 受养分，特别是 N 可用性的影响（Vicca et al.， 2012），但植物使用有机或无机 N 在多大程度上影响植物 CUE 尚未得到研究。然而，上述与不同 N 形式的吸收和同化有关的 C 成本差异理论上也会影响植物 CUE。因此，分析有机氮与无机氮营养对植物 CUE 的潜在影响可能为开发新的全球 C 模型提供重要信息。

在这里，我们从理论上（通过建模）和实验分析了不同 N 形式对植物生长和 C 和 N 分配的预期影响。我们轴向种植拟南芥 （Arabidopsis） 以研究根：芽分配、根毛形成和 CUE 如何比较两个 N 源 NO₃⁻ 和 l-gln。我们假设在有机氮源上生长的植物会表现出每根质量的氮吸收减少，根生物量和表面积增加，以及根质量分数增加。我们使用稳定同位素标记（¹³C 和 ¹⁵N）来量化植物对 N 和 C 来源的吸收和分布，从而能够评估 C 吸收对有机 N 表型发育的作用，并能够计算有机 N 吸收对植物 CUE 的影响。