Nutrition-mediated cell and tissue-level anatomy triggers the covariation of leaf photosynthesis and leaf mass per area

Plants in nutrient-poor habitats converge towards lower rates of leaf net CO2 assimilation (Aarea); however, they display variability in leaf mass investment per area (LMA). How a plant optimizes its leaf internal carbon investment may have knock-on effects on structural traits and, in turn, affect leaf carbon fixation. Quantitative models were applied to evaluate the structural causes of variations in LMA and their relevance to Aarea in rapeseed (Brassica napus) based on their responses to nitrogen (N), phosphorus (P), potassium (K), and boron (B) deficiencies. Leaf carbon fixation decreased in response to nutrient deficiency, but the photosynthetic limitations varied greatly depending on the deficient nutrient. In comparison with Aarea, the LMA exhibited diverse responses, being increased under P or B deficiency, decreased under K deficiency, and unaffected under N deficiency. These variations were due to changes in cell- and tissue-level carbon investments between cell dry mass density (N or K deficiency) and cellular anatomy, including cell dimension and number (P deficiency), or both (B deficiency). However, there was a conserved pattern independent of nutrient-specific limitations—low nutrient availability reduced leaf carbon fixation but increased carbon investment in non-photosynthetic structures, resulting in larger but fewer mesophyll cells with a thicker cell wall but a lower chloroplast surface area appressed to the intercellular airspace, which reduced the mesophyll conductance and feedback-limited Aarea. Our results provide insight into the importance of mineral nutrients in balancing the leaf carbon economy by coordinating leaf carbon assimilation and internal distribution.