Coordination of plant mitochondrial biogenesis: keeping pace with cellular requirements

Abstract

Plant mitochondria are complex organelles that carry out numerous metabolic processes related with the generation of energy for cellular functions and the synthesis and degradation of several compounds. Mitochondria are semiautonomous and dynamic organelles changing in shape, number, and composition depending on tissue or developmental stage. The biogenesis of functional mitochondria requires the coordination of genes present both in the nucleus and the organelle. In addition, due to their central role, all processes held inside mitochondria must be finely coordinated with those in other organelles according to cellular demands. Coordination is achieved by transcriptional control of nuclear genes encoding mitochondrial proteins by specific transcription factors that recognize conserved elements in their promoter regions. In turn, the expression of most of these transcription factors is linked to developmental and environmental cues, according to the availability of nutrients, light-dark cycles, and warning signals generated in response to stress conditions. Among the signals impacting in the expression of nuclear genes, retrograde signals that originate inside mitochondria help to adjust mitochondrial biogenesis to organelle demands. Adding more complexity, several nuclear encoded proteins are dual localized to mitochondria and either chloroplasts or the nucleus. Dual targeting might establish a crosstalk between the nucleus and cell organelles to ensure a fine coordination of cellular activities. In this article, we discuss how the different levels of coordination of mitochondrial biogenesis interconnect to optimize the function of the organelle according to both internal and external demands.

Keywords: coordination; mitochondrial biogenesis; mitochondrial dynamics; post-transcriptional gene regulation; retrograde signal; site II.

FIGURE 1

Mitochondrial dynamics. During the plant life cycle, mitochondria change in shape, size, and number, according to numerous stimuli provided by internal and external factors. Examples of processes related with changes in mitochondrial structure are shown in the lower part of the figure.

FIGURE 2

Site II elements are enriched in genes encoding mitochondrial proteins and are present in many nuclear genes encoding plastid and peroxisomal components. (A) Proportion of genes with site II elements among Arabidopsis nuclear genes encoding proteins destined to different cell compartments. Gene sets were taken from Law et al. (2012). Dual targeted proteins were taken from Xu et al. (2013b). The term “Random genes” refers to a set of 490 genes picked at random. (B) Location of site II elements respective to the transcription start site in different sets of genes. Vertical lines represent the first, second, and third quartiles, respectively.

FIGURE 3

Integrative view of different regulatory pathways involved in mitochondrial biogenesis. Mitochondrial biogenesis is regulated by numerous external factors, such as nutrient availability, environmental stimuli, light/dark conditions, diurnal cycle, and oxidative stress situations, among others (1). Mitochondrial biogenesis is also internally regulated by different stages of development, organ/tissue type, hormones, and cell energy and metabolic demands (2). The expression of a majority of nuclear genes for mitochondrial proteins is controlled by elements known as site II that are recognized by TCP transcription factors (3). Site II elements are either responsible for basal gene expression or modify the magnitude of the response under different growth conditions. Other transcription factors involved in the expression of nuclear genes encoding mitochondrial components belong to the bZip, AP2/ERF, and bHLH families (3). Evidence exists demonstrating the presence of proteins dual targeted to different organelles, which may act to coordinate the activities of these organelles (4,5). Physical and functional interactions between the inner membrane (IM) import machinery and complexes I, III, and IV help to adjust gene expression and protein assembly (6). Mitochondria generate signals to modify nuclear gene expression according to organelle demands (7).