Review
Carbon and nitrogen sensing and signaling in plants: emerging ‘matrix effects’

https://doi.org/10.1016/S1369-5266(00)00168-0Get rights and content

Abstract

Plants, like other organisms, have developed mechanisms that allow them to sense and respond to changes in levels of carbon and nitrogen metabolites. These mechanisms, in turn, regulate the expression of genes and the activities of proteins involved in C and N transport and metabolism, allowing plants to optimize the use of energy resources. Recent studies, which have involved molecular-genetic, genomic, and cell biological approaches, have begun to uncover the signals and components of C:N sensing and signaling mechanisms in plants. For sugar sensing, analysis of Arabidopsis mutants has revealed intersections with hormone and nitrogen signaling. For nitrogen sensing/signaling, recent progress has identified transcriptional and posttranslational mechanisms of regulation. In all, a complex picture is emerging in which C:N signaling systems are subject to a ‘matrix effect’ in which downstream responses are dependent upon cell-type, developmental, metabolic, and/or environmental conditions.

Introduction

The ability to sense carbon and nitrogen metabolites enables plants to regulate metabolism and development in response to their internal ratio of C to N. Possession of a sugar-sensing mechanism enables plants to turn off photosynthesis when C-skeletons are abundant. The N-sensing mechanism enables plants to turn off nitrate uptake and reduction when levels of reduced or organic N are high. The C:N-sensing mechanism enables plants to activate genes involved in N-assimilation when C skeletons are abundant and internal levels of organic-N are low, or to halt N-assimilation when levels of photosynthate are low or internal levels of organic-N are high. These C- and N-sensing mechanisms allow plants to efficiently utilize (or preserve) the energy needed to drive the transport and metabolism of C and N.

Mechanisms for sugar and N sensing are also found in bacteria and yeast. Molecular-genetic studies in these unicellular organisms have revealed remarkably complex sensing/signaling systems. In yeast for example, there are at least three independent sugar-sensing/-signaling systems. C:N signaling pathways in plants will surely have additional complexities that are associated with a multicellular organism. For example, C and N signals serve to coordinate the metabolism and transport of these metabolites between source and sink tissues throughout the life cycle, and may also serve as metabolic signals that integrate environmental inputs, such as light, with internal regulators, such as hormones. A complex picture is emerging in which C:N signaling networks are subject to a ‘matrix effect’ in which certain functions or interactions only occur under situations defined by species, cell-type, developmental stage, metabolic status, or environmental conditions. A good example of the matrix effect was revealed by recent findings showing that certain sugar responses are dependent on N status and vice versa. This review emphasizes important recent progress in defining sugar and N regulatory networks in plants and how they intersect, and highlights examples of matrix effects.

Section snippets

Sucrose sensing in plants

Both sucrose and glucose can initiate changes in gene regulation. Because sucrose is readily hydrolyzed to glucose and fructose, however, sucrose-specific signaling effects have been difficult to elucidate. Recent experimental evidence indicates the existence of sucrose-specific regulatory pathways affecting transcription and translation in plants. These pathways include the sucrose-specific gene induction of the promoters of patatin and of phloem-specific rolC 1•; the repression by sucrose of

Crosstalk of sugar signaling with hormonal pathways

Much progress has been made recently in revealing crosstalk between sugar signaling and hormone signals such as ethylene, cytokinin, and abscisic acid (ABA) 11, 20, 21•, 22, 23. In particular, it has been discovered that ABI4 (ABA-INSENSITIVE4) is a signaling component that is shared between ABA and glucose signaling during seedling development 21•, 22, 23. Nevertheless, questions remain as to how, when, and where these interactions take place 24. An interesting example of cross-talk concerns

Conclusions

Carbon and nitrogen sensing and signaling are important mechanisms that enable an organism to regulate its metabolism and development in response to nutrient status. Such signaling systems have been the subject of elegant studies in unicellular organisms, such as yeast and E. coli, for decades. In these systems, the signaling systems that are being unraveled are multiple and complex. Equivalent studies in plants are more recent, and early attempts to define the nutrient signals and components

Acknowledgements

The authors would like to thank Laurence Lejay, Brandon Moore, and Zhanguo Xin for their critical reading of the manuscript.

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

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