Vernalization, Competence, and the Epigenetic Memory of Winter

Abstract

Vernalization is the process by which prolonged exposure to cold temperatures promotes flowering. Over the past century, this process has been studied extensively at the physiological level. Recent studies have provided some insight into the molecular basis of vernalization. The rich history of vernalization research has been discussed in detail in many reviews (Chouard, 1960; Lang, 1965; Bernier et al., 1981). I will briefly summarize some highlights and classic experiments that I would like to relate to recent molecular advances. The first papers describing exposure to cold as the specific climatic aspect of winter that was necessary for flowering in some species were published in the latter half of the 19th century. However, the work of Gassner (1918)is usually cited as the first report that a wide range of plant species require cold exposure to flower (Chouard, 1960; Lang, 1965). Examples of Plants Requiring Vernalization. (A) A biennial cabbage (Brassica oleracea) variety with an obligate vernalization requirement that had been growing for five years without cold exposure. The small plant in my daughter's hands is a summer-annual variety of B. oleracea that flowers rapidly without vernalization. (B) and (C) Summer annual and vernalization-requiring types of henbane (B) and Arabidopsis (C). In both examples, a single-dominant gene is responsible for the vernalization-requiring habit. All plants were grown in long days (inductive photoperiods) without vernalization. The rapid-flowering summer annuals (which have initiated flowering) are at left and the winter-annual types at right. (Henbane images courtesy of Jan Zeevaart.) The distinction between summer annuals and winter annuals or biennials is not always absolute. It is possible that genetically identical plants could behave as summer annuals in one location and as winter annuals in a different location with a different climate. Furthermore, these classifications do not imply fundamental differences in the mechanisms that control flowering. In Arabidopsis, for example, single-gene changes can convert plants without a vernalization requirement into plants that have either a quantitative or obligate requirement or vice versa; therefore, the relevant molecular differences between plants in various categories can be minor. Many winter annuals and biennials become established in the fall, taking advantage of the cool and moist conditions optimal for their growth. The vernalization requirement of such plants prevents flowering until spring has actually arrived. Weather is often variable, so for a vernalization requirement to work as intended, plants must not only sense cold exposure but also have a mechanism to measure the duration of cold exposure. For example, if a plant is exposed to a short period of cold in the fall season, followed by a return of warm temperatures later that fall or in early winter, it is important for the plant not to perceive the brief exposure to cold and the following warm weather as spring. One mechanism to determine that spring has in fact arrived is to measure the duration of cold and to permit flowering only after a period of cold that is sufficient to ensure that winter has passed. Sensing the increasing daylengths in the spring can also play a role. In many perennial species, the release of buds from dormancy only after perception of a sufficient duration of cold exposure is, like vernalization, designed to measure the duration of a winter season. Processes that require prolonged exposure to cold, such as vernalization and the cold-induced release of bud dormancy, stand in contrast with cold acclimation—a process designed to respond to cold as rapidly as possible (Thomashow, 2001). Within a given species, there can be variation in the extent to which vernalization affects flowering time. In some species there are varieties that require vernalization and others that do not, such as winter and spring varieties of cereals (e.g., winter wheat and spring wheat). In fact, the term vernalization comes from studies of flowering in cereals. The infamous Russian geneticist Trofim Lysenko, who studied the effect of cold on flowering, coined the term jarovization to describe what we now call vernalization. Spring cereals are called jarovoe in Russian (derived from Jar, the god of spring), and cold exposure causes a winter cereal to behave like a jarovoe (i.e., to flower rapidly). Jarovization was translated from Russian into vernalization; vernal is derived from the Latin word for spring, vernum (Chouard, 1960). A useful definition of vernalization is provided in Chouard's review (1960, p. 193): “the acquisition or acceleration of the ability to flower by a chilling treatment.” Two types of experiments demonstrate that this acquisition or acceleration is occurring at the shoot apex. One is to locally chill only certain parts of the plant. Another is to graft shoot tips: In most species, if a vernalized shoot tip is grafted to nonvernali