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Overall, our work demonstrates that, independent of the soil N conditions, increasing N transport to leaves provides a promising approach for optimizing N use in support of C fixation as well as for sink development and oilseed yield.

Abstract The coordinated distribution of nitrogen to source leaves and sinks is essential for supporting leaf metabolism while also supplying sufficient nitrogen to seeds for development.

This study aimed to understand how regulated amino acid allocation to leaves affects photosynthesis and overall plant nitrogen use efficiency in Arabidopsis ( Arabidopsis thaliana ) and how soil nitrogen availability influences these processes.

Arabidopsis plants with a knockout of AAP2, encoding an amino acid permease involved in xylem-to-phloem transfer of root-derived amino acids, were grown in low-, moderate-, and high-nitrogen environments.

We analyzed nitrogen allocation to shoot tissues, photosynthesis, and photosynthetic and plant nitrogen use efficiency in these knockout plants.

Our results demonstrate that, independent of nitrogen conditions, aap2 plants allocate more nitrogen to leaves than wild-type plants.

Increased leaf nitrogen supply positively affected chlorophyll and Rubisco levels, photosynthetic nitrogen use efficiency, and carbon assimilation and transport to sinks.

The aap2 plants outperformed wild-type plants with respect to growth, seed yield and carbon storage pools, and nitrogen use efficiency in both high and deficient nitrogen environments.

Overall, this study demonstrates that increasing nitrogen allocation to leaves represents an effective strategy for improving carbon fixation and photosynthetic nitrogen use efficiency.

The results indicate that an optimized coordination of nitrogen and carbon partitioning processes is critical for high oilseed production in Arabidopsis, including in plants exposed to limiting nitrogen conditions.

Nitrogen (N) is an essential nutrient that plants require for the synthesis of amino acids, proteins, and many other important metabolites.

Consequently, the amount of N that is assimilated and distributed from roots to source leaves and finally to developing sinks, like fruits and seeds, has significant consequences for plant metabolism and growth.

In fact, Rubisco, the primary enzyme in C fixation, alone can account for up to 30 of the total N and 60 of the soluble proteins in mature source leaves ( Sage et al., 1987; Makino and Osmond, 1991; Osaki et al., 1993; Warren et al., 2000 ).

Accordingly, photosynthetic nitrogen use efficiency (PNUE) is related to the proportion of leaf N used for C fixation per unit of leaf area ( Poorter and Evans, 1998; Onoda et al., 2004; Warren and Adams, 2006 ).

Plants must balance N allocation in support of leaf metabolism with supplying sufficient N to developing sinks.

However, strategies for crop improvement generally have not integrated PNUE with plant NUE ( Hirel et al., 2007; Kant et al., 2012 ).

NUE is determined by the seed yield relative to N supply and generally is divided into two major components, nitrogen uptake efficiency (NUpE) and nitrogen utilization efficiency (NUtE).

In most plant species, N partitioning within the plant and to sinks occurs in the form of amino acids, and recent studies have demonstrated that altering amino acid transport processes from leaves to seeds impacts N and C assimilation, seed development ( Rolletschek et al., 2005; Schmidt et al., 2007; Weigelt et al., 2008; Zhang et al., 2010, 2015; Carter and Tegeder, 2016; Santiago and Tegeder, 2016, 2017 ), and overall plant NUE ( Perchlik and Tegeder, 2017 ).

Here, it was hypothesized that regulated amino acid allocation from the root to leaves influences PNUE and also affects plant NUE.

Root-synthesized amino acids are transported in the xylem to mature source leaves, where they are used for metabolism, stored, or loaded into the phloem to supply sinks with N ( Atkins et al., 1983 ).

In Arabidopsis ( Arabidopsis thaliana ), AMINO ACID PERMEASE2 (AAP2) is involved in this xylem-to-phloem transfer step ( Zhang et al., 2010 ), and knockout of AAP2 results in decreased N delivery to seeds and reduced seed protein levels ( Zhang et al., 2010 ).

However, in these aap2 mutants, amino acid allocation to leaves was increased, positively affecting photosynthesis and Suc transport to sinks.

This resulted in higher seed yields and seed oil levels ( Zhang et al., 2010 ).

This study aimed to resolve how regulated amino acid allocation to leaves impacts photosynthesis and PNUE, how plant N and C status and overall NUE are affected, and how soil N availability influences these processes.

It is demonstrated that, independent of the amount of N nutrition, aap2 plants move significantly more N to leaves, promoting leaf growth and photosynthetic surface area.

In addition, shifts in leaf N pools and rates of electron transport occurred in favor of photosynthesis, resulting in enhanced C fixation and PNUE.

Furthermore, the transgenic plants displayed improved NUpE and significant increases in total shoot N and C.

Together, the increased amino acid delivery to aap2 leaves and a subsequent enhanced sink C supply resulted in higher NUE, including under N stress conditions.

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