Comparing Potato Tuberization and Sprouting: Opposite Phenomena?

American Journal of Potato Research, Jul/Aug 2004 by Vreugdenhil, Dick

ABSTRACT

The regulation of tuber formation and tuber sprouting are compared. As a starting point it is hypothesized that these two phenomena are opposite to each other. This idea is tested from three points of view: hormonal regulation, gene expression, and carbohydrate metabolism. It is concluded that there is only limited evidence to support the hypothesis. On the contrary, several examples are given indicating that similar mechanisms might be operative during tuber formation and tuber sprouting.

RESUMEN

Se comparan los métodos de formación y brotamiento del tubércule. Se parte de la hipótesis que estos fenómenos son opuestos entre sí. Esta idea ha sido probada desde tres puntos de vista: regulación hormonal, expresión de los genes y metabolismo de carbohidratos. Se concluye que sólo existe evidencia limitada para defender estas hipótesis. Por el contrario se dan varios ejemplos que indican que mecanismos similares podrían ser operativos durante la formación y brotamiento del tubérculo.

Accepted for publication 6 February 2004.

ADDITIONAL KEY WORDS: carbohydrate metabolism, gene expression, hormones, Solanum tuberosum

This paper was originally presented as part of a symposium entitled "Recent Advances in the Physiology of Tuberization and Tuber Dormancy." The symposium was held on 11 August 2003, by the Potato Association of America, in Spokane, WA.

INTRODUCTION

Tuber formation in potatoes comprises a switch in the direction of growth of the stolon, viz., from longitudinal to radial. When a tuber sprouts, an elongating structure (the sprout) forms from the swollen organ. This alternating sequence of events in the direction of growth, viz., longitudinal-radial-longitudinal, raises the question: Is the regulation of tuber sprouting (partly or completely) the reverse of the regulation of tuber initiation? A positive answer to this question is suggested by observations that environmental factors unfavorable for tuber development, such as high temperatures, may result in premature sprouting. To examine other possible parallels, we decided to compare in more detail physiological and molecular changes occurring during the processes of tuber initiation and sprouting.

This topic has been discussed before by Claassens and Vreugdenhil (2000). Their paper focussed mainly on hormonal regulation and on carbohydrate metabolism. The conclusion from this paper was "when comparing tuber induction and the breaking of dormancy, hormonal activities are only partly the reverse, while for carbohydrates and enzyme activities some clear reversed trends were found."

New data have become available on an aspect receiving only little attention in the previous review, viz., gene expression, and also on biochemical processes (carbohydrate metabolism). The current state of knowledge on hormonal regulation will also briefly be updated.

HORMONES

The last few years several papers have reviewed the state of knowledge on the role of hormones in the regulation of tuber formation and in tuber dormancy (Jackson 1999; Vreugdenhil and Sergeeva 1999; Claassens and Vreugdenhil 2000; Suttle 2000). With respect to tuber induction gibberellins are clearly regulating this developmental process, i.e., high levels of this hormone prevent tuber formation. Carrera et al. (2000) found that transgenic plants overexpressing a GA-20 oxidase and showing increased levels of gibberellins exhibited premature sprouting. This observation further supports the stimulating role of gibberellins in sprout development.

Cytokinins have long been suggested to be involved in tuberization. Recently a transgenic approach further supported a role for cytokinins in tuber induction: a promoterless ipt gene (a bacterial cytokinin biosynthetic gene) was inserted into tobacco and was found to be specifically expressed in axillary buds tubers (Guivarc'h et al. 2002). This transgenic tobacco line exhibited swollen internodes that resembled tubers and were filled with starch grains. Immuno-localization studies indicated increased levels of cytokinins in the buds of these plants, strongly suggesting that cytokinins may act as positive triggers to stimulate tuber formation, even in a species not normally forming tubers (Guivarc'h et al. 2002).

Suttle and Banowetz (2000) and Suttle (2001) reported that; levels of the cytokinin cis-zeatin increased during storage and that the sensitivity of the tubers towards exogenous cisand trans-zeatin, determined as sprouting of the tubers, also increased during storage. This is consistent with a role of zeatin in regulation of potato tuber dormancy.

It should be noted that these recent reports indicate that both tuberization and the ending of tuber dormancy are associated with high levels of and/or sensitivity towards cytokinins. This is consistent with earlier findings, but does not support; the hypothesis that the regulation of both processes is opposite to one each other at least not for cytokinins.

The role of cytokinins might, be primarily in the regulation of cell division, a necessary step both during tuberization and during sprouting. Cytokinins have been shown to be involved in cell cycle control (Riou-Khamlichi et al. 1999), and the buds of the ipi-transgenic tobacco plants showed changes in cell cycle related parameters (Guivarc'h et al. 2002). This is consistent with the finding of Verhees et al. (2002) showing up-regulation of expression of cell-cycle-related genes during tuber formation and during sprouting (further discussed below).