Friends in Arms: Flavonoids and the Auxin/Cytokinin Balance in Terrestrialization

Abstract

Land plants survive the challenges of new environments by evolving mechanisms that protect them from excess irradiation, nutrient deficiency, and temperature and water availability fluctuations. One such evolved mechanism is the regulation of the shoot/root growth ratio in response to water and nutrient availability by balancing the actions of the hormones auxin and cytokinin. Plant terrestrialization co-occurred with a dramatic expansion in secondary metabolism, particularly with the evolution and establishment of the flavonoid biosynthetic pathway. Flavonoid biosynthesis is responsive to a wide range of stresses, and the numerous synthesized flavonoid species offer two main evolutionary advantages to land plants. First, flavonoids are antioxidants and thus defend plants against those adverse conditions that lead to the overproduction of reactive oxygen species. Second, flavonoids aid in protecting plants against water and nutrient deficiency by modulating root development and establishing symbiotic relations with beneficial soil fungi and bacteria. Here, we review different aspects of the relationships between the auxin/cytokinin module and flavonoids. The current body of knowledge suggests that whereas both auxin and cytokinin regulate flavonoid biosynthesis, flavonoids act to fine-tune only auxin, which in turn regulates cytokinin action. This conclusion agrees with the established master regulatory function of auxin in controlling the shoot/root growth ratio.

Keywords: antioxidants; auxin; cytokinin; flavonoids; oxidative stress; shoot/root ratio; symbiosis; terrestrialization.

Figure 1

The auxin/cytokinin ratio and water and nutrient availability. Under optimal water and nutrient availability, auxin action decreases with a concomitant increase in cytokinin action, which increases the shoot/root growth ratio and leads to reproduction. A high auxin/cytokinin ratio would be suboptimal under these conditions, as it would lead to the needless allocation of carbon to root growth. Under water and nutrient deficiency conditions, auxin action is increased and cytokinin action is decreased, which ensures plant survival and reproduction, albeit at a lower rate. A high cytokinin/auxin ratio would be lethal under these conditions; vigorous shoot growth would cause potentially deadly water loss, and the insufficient allocation of carbon flow to roots would impede an increase in root development needed to acquire adequate amounts of water and nutrients.

Figure 2

Auxin and cytokinin interactions with flavonoids in shoots and roots. Cytokinin, the promoter of shoot growth, upregulates the biosynthesis of anthocyanins in shoots, strengthening the antioxidative system poised to combat the excess of ROS generated, for example, by photosynthesis or by the action of environmental stressors. Auxin in roots upregulates the biosynthesis of flavonols, which modify auxin action by inhibiting auxin transport and counteracting auxin-induced ROS accumulation. The flavonoid-dependent inhibition of auxin transport is not restricted to roots—it also acts in shoots to shape petiole angle and leaf nastic development. In addition, flavonol synthesis is environmentally controlled, thus linking environmental fluctuations to changes in auxin action for optimal environmental adaptation.

Figure 3

Model illustrating the auxin/cytokinin ratios during the establishment of AMF symbiosis from the perspective of adaptive control of the shoot/root growth ratio. As long as the plant perceives phosphate deficiency in the soil, the rate of AMF symbiosis establishment is high, mirroring a low shoot/root growth ratio and the allocation of resources towards root growth and fungal colonization. Under phosphate-deficient conditions, auxin action is high, which represses cytokinin action and shoot growth in favor of root growth and symbiosis. Under phosphate-sufficient conditions, auxin action is reduced, and cytokinin action is released to promote shoot growth, inhibit root growth, and suppress AMF symbiosis. Flavonoids play an essential role in this process, as they promote several stages of this symbiotic interaction.

Figure 4

Model representing the actions of auxin and cytokinin on root nodulation from the perspective of adaptive control of the shoot/root growth ratio. As long as the plant perceives nitrogen deficiency in the soil, nodulation frequency is high, mirroring a low shoot/root growth ratio and the allocation of resources towards root growth and nodulation. Under nitrogen-deficient conditions, auxin action is high, which represses cytokinin action and shoot growth in favor of root growth and nodulation. Under nitrogen-sufficient conditions, auxin action is reduced, and cytokinin action is released to promote shoot growth and inhibit root growth and nodulation. This mechanism ensures optimal resource allocation for shoot growth and reproduction under optimal nitrogen conditions. Flavonoids play an essential role in this process, as they promote several stages in this symbiotic interaction and thus help with the auxin-dependent promotion of nitrogen fixation.