Carbon (C) and Nitrogen (N) are two essential macronutrients that are fundamental for the survival of all organisms including plant growth and development. Shoots and leaves fix C through photosynthesis into carbohydrate (sugars and starches), the primary source of energy that is required for growth. By contrast, nitrogen along with water and other nutrients (phosphorous, potassium, secondary- and micro-nutrients) is taken up from the soil by roots and is a major nutrient for growth as it is needed to synthesise amino acids, which are the building elements of protein, nucleotides, chlorophyll, and numerous other metabolites and cellular components. At the global scale, the interactions between the N and C cycle are key players in Earth’s climate and other planetary processes [1]. Many decades of research has shed light into the various aspects of how C and N availability and allocation coordinates growth and plant response to environment (biotic and abiotic stresses) and it is one on the major questions in many areas of plant biology, from general physiology to cell biology, from molecular biology to ecology and stress biology. Therefore, not only to understand plant growth and development but also how plants response to environment, it is important to “Follow C and N” and this core theme is well-deserved to be in the spotlight.

C is acquired through photosynthesis and carbon assimilation principally in leaf mesophyll cells. For distribution to distal tissues, fixed carbon must move out of the photosynthetic cells and into the phloem. To distribute resources such as C and N, plants have a vasculature composed of phloem and xylem. The xylem conducts water, N and minerals from the roots up to the shoots. The distribution of carbonand nitrogen-containing compounds occurs by their loading into the phloem and transporting them from the photosynthetic “sources” (predominantly leaves) to the heterotrophic “sinks” (meristems, roots, flowers, and seeds) where these compounds is unloaded [2]. This process is called carbon partitioning in which assimilates are distributed throughout the plant body from photosynthetic tissues. Sucrose is synthesised in leaf mesophyll cells and diffuses cell-to-cell through plasmodesmata toward the phloem which is the specialised tissue involved in long-distance sucrose transport via sucrose- and monosaccharide- transporters [2-5]. However, it has also been shown that down-regulating a sucrose transporter gene does not inhibit phloem loading [6]. Prior to sucrose be transported in the phloem, it must effuse from inside the cell into the cell wall proactively and recently it was shown that sucrose effluxers play a key role in this process [7]. Several other transporters/channels of sucrose, K⁺ and water have been characterised for their contribution to the sucrose transport in the phloem [2-5]. Apart from transporters, there are other proteins are also involved in phloem loading and carbohydrate partitioning [8,9]. Besides C fixation through photosynthesis, the proper and efficient allocation of carbohydrates is also fundamental for plant growth. On the other hand, N availability is a major limiting factor for plant growth, development and productivity. Biologically available N forms (e.g. nitrate or ammonia) are in short supply in nature as well as in agricultural systems. N removed from the soil in crop products must be replaced to sustain agricultural productivity. N fertilisers (e.g. urea and ammonium nitrate) are the main sources of N applied to crops and represent up to 50% of the operational costs in agriculture [10]. Furthermore, unutilised N (more than half of the applied N) is not used by crops and hence is lost into the soil or is released to the atmosphere as nitrogen gases such as nitrous oxide which is the third contributor to global warming and excess N can cause eutrophication of terrestrial and aquatic systems.

C and N metabolism are intimately linked. N deficiency decreases C assimilation, while C starvation reduces N utilisation in plants. N deficiency therefore affects, to various extents, primary photosynthesis, sugar metabolism and/or carbohydrate partitioning between source and sink tissues [11]. N along with water and other nutrients are principally acquired by roots. C allocation below ground is often greater than that allocated above ground [12]. N metabolism is severely impaired when photosynthesis rate is decreased [13]. On the other hand, photosynthesis rate is significantly reduced when N availability is limited [14]. Therefore, the balance between C and N is critical to ensure optimal nutrient utilisation for growth, development and response to environment (biotic and abiotic stresses) via complex coordinated metabolic responses and signalling pathways. C and N availability and allocation is also a major topic of ecological interest [15].

However, the molecular mechanisms underlying the co-regulation of C and N are not understood. Can a plant sense the C/N ratio (or balance)? If so, what is the molecular mechanism(s) involved in this process? These are some of the key questions still remain elusive. Despite this, it is well accepted that C and N are not only important energy sources and structural components, but also central regulatory molecules controlling gene expression, metabolism, physiology, and growth and development [16-19].

Glucose, sucrose and trehalose have been suggested to act as C signals [20,21]. A glucose-specific sensor HEXOKINASE1 has been identified [22]. Despite a decade-long search, a sucrose-specific sensor remains to be discovered, although sucrose-specific pathways have been demonstrated. Sucrose-specific signalling is difficult to study since sucrose is readily hydrolysed into hexoses, which are powerful signalling molecules as well [23]. Several transcriptional regulators are implicated in coordinating C signalling. Arabidopsis transcription factors bZIP and master clock control CIRCADIAN CLOCK ASSOCIATED1 are well known transducers of sucrose-specific signals [24-26].

For N signalling, the low-affinity NITRATE TRANSPORTER 1.1 protein is identified as involved in both nitrate perception and transport. Additionally, the high-affinity NITRATE TRANSPORTER 2.1 (NRT2.1) is one of several primary nitrate response genes that show a rapid induction of gene expression in response to nitrate treatments independent of protein synthesis. NRT2.1 represses lateral root initiation in response to nutritional cues by acting either as a nitrate sensor or signal transducer [27]. Similarly, the role of AMMONIUM TRANSPORTER 1.3 in regulating lateral root branching in response to ammonium is independent of ammonium transport, suggesting a signalling role for this transporter [28]. Several regulatory factors involved in N responses have been identified. These include a MADS box transcription factor ARABIDOPSIS NITRATE REGULATED 1 which promotes lateral root development in response to nitrate, a NIN-LIKE PROTEIN 7 which is required for normal nitrate regulation of N-assimilatory genes, members of the LATERAL ORGAN BOUNDARY DOMAIN (LBD37/38/39) which repress anthocyanin biosynthesis and many known N-responsive genes, ELONGATED HYPOCOTYL 5 which positively regulates NITRATE REDUCTASE 2 and negatively regulates NRT1.1 and SQUAMOSA PROMOTER BINDING PROTEIN–LIKE 9 which negatively regulates nitrite and nitrate reductases.

Interestingly, some of the transcription factors such as bZIP and CIRCADIAN CLOCK ASSOCIATED 1 which regulated by C are also known to be regulated by N and may function as integrators of C and N signalling [26,29]. It is also known that root system architecture, which is critical for N uptake and regulated by N, is also regulated by sucrose uptake in the aerial tissues [30]. However, the underlying molecular mechanism(s) for how plant senses the C/N ratio and mediates growth, development and response to environment are remains to be identified.

The world population is estimated to reach nine billion by mid-twenty-first-century (United Nations, http://esa.un.org/unpd/wpp/index.htm). The increased demand for food will impose a substantial strain on agriculture. Urgency is required to develop more sustainable, economically-viable “Second Green Revolution” crops for food production with higher photosynthesis rate and better N use efficiency. To achieve this, it is necessary to understand the molecular mechanisms underlying the coordination between C and N metabolism and regulation. Notably, establishment of a holistic view of how plants control C/N ratio and metabolism coordinately at the whole plant level can’t be overlooked.

This work was supported by the ARC grant (DP120101893).