Multiple Signaling Pathways Control Tuber Induction in Potato

Abstract

Potatoes (tubers of Solanum tuberosum) are grown and eaten in more countries than any other crop, and in the global economy they are the fourth most important crop after the three cereals maize, rice, and wheat. Therefore, research into potato tuber initiation and development, which enables our understanding and possible manipulation of these processes, is of great relevance. In addition to improving the yield and quality of potato harvests and increasing resistance to pathogen infection, research is also directed at improving the nutritional content of the tuber, and “pharming” which is removing the starch in the potato tuber and instead producing organic compounds such as proteins that are too expensive or cannot be produced in bacterial or yeast culture systems. Research on potatoes has many advantages in that they are easily transformable and therefore amenable to genetic manipulation, and can be propagated rapidly both in tissue culture and through cuttings. Also, microtubers can be induced to form in tissue culture and are used in experimental systems in some laboratories. Other laboratories have used stem cuttings as small models of the whole plant. Last but not least, the potato is very closely related to the tomato, for which there is a good genetic map. The main drawback to the use of potatoes in research is the fact that most potato species are polyploid, which means that classical genetic experiments cannot be performed. Solanum demissum plants grown in noninducing long-day (left) or inducing short-day (right) conditions. The tuberization response of cuttings that have been induced to differing degrees. From left to right, noninduced (no stolon or tuber) to strongly induced (sessile tuber). Photo courtesy of E. Ewing (Cornell University, Ithaca, NY). Tubers can actually form on other parts of the plant above ground, normally from axillary nodes on the stem, and in specific circumstances they can even form from flowers (Ewing and Struik, 1992). These aerial tubers are usually formed only on injured or diseased plants, where translocation of assimilates below ground has been prevented, or in plants grown in very strong inducing conditions. This Update cannot possibly summarize all of the knowledge available about potato tuberization, much of which can be found elsewhere (Li, 1985; Ewing and Struik, 1992, and refs. therein). Therefore, it will principally focus on the role of the environment and possible hormonal signals involved in the induction of tuberization rather than on the postinduction processes such as starch and storage protein accumulation that occur during tuber formation. There are many factors that affect tuber formation—even the bacteria living in the root zone are reported to have an influence—but nitrogen levels, temperature, and light have the greatest effect. Although the overall effects of various environmental factors are generally consistent, the genotype and physiological age and state of the plant (e.g. whether still attached to the mother tuber or derived from cuttings) can cause considerable variations in the degree to which a plant responds to a particular environmental stimulus. Analyses have been performed on a population segregating for the ability to tuberize under a specific set of conditions to try to identify quantitative trait loci that affect tuberization (Van den Berg et al., 1996). Elegant experiments by Krauss and co-workers (for review, seeKrauss, 1985) demonstrated that tuberization could readily be manipulated by altering the supply of nitrogen (either ammonium or nitrate ions) to the plant. Whereas previous studies had looked at the effect of high doses of nitrogen fertilizer on field-grown plants, Krauss and co-workers grew the plants in liquid media (hydroponic culture) in which the level of nitrogen supplied to the plant could be precisely controlled. They found that a continuous supply of between 1 and 3 mm nitrogen completely inhibited or severely delayed tuberization in otherwise inducing conditions. However, interrupting the nitrogen supply by putting the plants temporarily in nitrogen-free media for 4 to 6 d allowed tuberization to occur. If the plants are put into “excessive” nitrogen supply after they have started tuberizing, then tuber formation will cease and stolon growth may be resumed. Removal of the nitrogen from the media will then cause initiation of a second tuber from this stolon (secondary growth). Repeated cycles of high nitrogen/nitrogen withdrawal can result in the formation of “chain tubers,” demonstrating that nitrogen levels play an important role in the control of tuber formation. It is interesting that high nitrogen supply to the leaf did not prevent tuberization, even though the nitrogen content of the plants was comparable to those receiving high nitrogen through the roots. Furthermore, reducing nitrogen levels in normally noninducing conditions such as LD or high temperatures (see below) will not result in tuberization, ind