Biological processes involved in photorespiratory and photosynthetic metabolism operate concurrently and affect the interplay between carbon and nitrogen assimilation reflected in plant growth. Experimental evidence has indicated that photorespiratory metabolism has a wide-ranging influence not only on other principal metabolic pathways but also on a multitude of signalling cascades. Therefore, accurate quantitative models of photorespiration can provide a means for predicting and in silico probing of plant behaviour at various levels of the system. We first present a comprehensive classification of current models of photorespiratory metabolism developed within the existing carbon-centric modelling paradigm. We then offer a perspective for modelling photorespiratory metabolism by considering the coupling of carbon and nitrogen metabolism in the context of compartmentalised, genome-scale metabolic models of C3 plants. In addition, we outline the challenges stemming from the need to consider plant metabolic and signalling pathways in assessing the still controversial role of photorespiration and to confront the devised models with the ever-increasing amounts of high-throughput data.