The Molecular and Genetic Control of Leaf Senescence and Longevity in Arabidopsis

Pyung Ok Lim*; Hong Gil Nam    National Research Laboratory of Plant Molecular Genetics, Division of Molecular and Life Sciences, Pohang University of Science and Technology Pohang, Kyungbuk, 790-784, Korea
* Current address: Department of Science Education, Cheju National University, Jeju-si, Jeju 690-756, Korea

The life of a leaf initiated from a leaf primordium ends with senescence, the final step of leaf development. Leaf senescence is a developmentally programmed degeneration process that is controlled by multiple developmental and environmental signals. It is a highly regulated and complex process that involves orderly, sequential changes in cellular physiology, biochemistry, and gene expression. Elucidating molecular mechanisms underlying such a complex, yet delicate process of leaf senescence is a challenging and important biological task. For the past decade, impressive progress has been achieved on the molecular processes of leaf senescence through identification of genes that show enhanced expression during senescence. In addition, Arabidopsis has been established as a model plant for genetic analysis of leaf senescence. The progress on the characterization of genetic mutants of leaf senescence in Arabidopsis has firmly shown that leaf senescence is a genetically controlled developmental phenomenon involving numerous regulatory elements. Especially, employment of global expression analysis as well as genomic resources in Arabidopsis has been very fruitful in revealing the molecular genetic nature and mechanisms underlying leaf senescence. This progress, including molecular characterization of some of the genetic regulatory elements, are revealing that senescence is composed of a complex regulatory network. In this review, we will present current understanding of the molecular genetic mechanisms by which leaf senescence is regulated and processed, focusing mostly on the regulatory factors of senescence in Arabidopsis. We also present a potential biotechnological implication of leaf senescence studies on the improvement of important agronomic traits such as crop yield and post-harvest shelf life. We further provide future research prospects to better understand the complex regulatory network of senescence. © 2005, Elsevier Inc.

I Introduction

Leaf senescence is most typically observed in the leaves at autumn and during the death process of monocarpic plants, such as rice and crysanthemum. Like other senescence events, leaf senescence is the final phase of development, during which cells undergo distinct metabolic and structural changes leading to cell death (Noodén, 1988). Leaf senescence and its following death is perhaps one of the most dramatic developmental phenomena encountered in nature. Thus, leaf senescence has been a favorite topic for poets and artists from ancient times and has also evoked curiosity about its underlying mechanisms. Besides artistic instinct and scientific curiosity, leaf senescence also stimulates strong interest in its practical application in improving plant productivity and storage characteristics, which should become fairly feasible by modifying the senescence process.

Senescence in higher plants, including leaf senescence, is a type of programmed cell death (PCD) that occurs by a genetic program as a part of a developmental process (Nam, 1997). PCD in higher plants occurs throughout development of most organs and can be triggered by developmental as well as environmental factors, such as pathogen infection and physical injury. While other PCDs such as hypersensitive response involve rather localized cell death, cell death during senescence is mostly observed in a broad area of plant bodies, for example, in organs such as leaves, petals, fruits, or plant bodies as a whole. Cell death during senescence also occurs more slowly than in other PCDs, where cell death occurs more acutely. The slower cell death during senescence is, in part, associated with efficient remobilization of nutrients that are degraded during senescence.

For the clarity of this chapter, we distinguish the term “senescence” and “developmental aging” in plants. The term “senescence” is applicable to a process that leads to death of a cell, an organ, or a whole plant and occurs at the final stage of development. By contrast, developmental aging occurs throughout development, from initiation of a leaf primordium throughout senescence and death; conceptually, developmental aging would determine when senescence starts but it is not itself senescence.

Plants, like other organisms, show two types of senescence: mitotic senescence and postmitotic senescence (Gan, 2003). Meristematic cells can undergo a given number of mitotic divisions to produce organs such as leaves and flowers. Loss of capacity for further cell divisions in the meristematic cells is called mitotic senescence or replicative senescence. This type of senescence is also observed in yeast and mammalian cells. In contrast, postmitotic senescence occurs in mature organs such as leaves and petals. Cells in these organs rarely undergo cell division, but these cells undergo cell growth, maturation, senescence, and ultimately, death. In this chapter, we focus our attention mostly on leaf senescence, a type of postmitotic senescence.

A leaf is initially formed as a leaf primordium that is derived from the shoot apical meristem. After growth and maturation into a photosynthetic organ through a series of cell division and differentiation steps, the leaf organ undergoes the final stage of development, namely, senescence. During senescence, leaf cells undergo dramatic changes in cellular metabolism and the sequential degeneration of cellular structures (Nam, 1997; Noodén, 1988). The cellular degeneration process occurs in an orderly manner, beginning with the chloroplast. The mitochondria and the nucleus remain intact until the final stages of leaf senescence. The metabolic changes include loss of photosynthetic activities and hydrolysis of macromolecules that have been accumulated during the growth phase. These degenerative activities occur concomitantly with a massive remobilization of the hydrolyzed molecules to the growing parts of plants, such as young leaves, developing seeds, and fruits. Leaf senescence is therefore an important phase in the plant life cycle that critically contributes to the fitness of plants, ensuring better survival of plants and optimal production of their offspring (Nam, 1997; Noodén, 1988).

Since 1995, some extensive research has been conducted to understand the molecular genetic mechanisms underlying the leaf senescence process by identifying mutants that show altered senescence processes and genes that show altered expression during senescence, using the model plant Arabidopsis. Analyses of these mutants and genes are beginning to expand our understanding of the nature and regulation of leaf senescence. In this chapter, we present current understanding of the molecular genetic mechanisms by which senescence is regulated and processed, using results obtained mostly from the model plant Arabidopsis. We further provide a few points for future research trends.

II Arabidopsis as a Model Plant for Studying Leaf Senescence

Extensive genomic resources are available for Arabidopsis, which makes it useful for the rapid identification and functional analysis of senescence-regulated genes. In addition to the general advantage of Arabidopsis as a molecular genetic model plant, the Arabidopsis leaf has a short life cycle, readily distinguishable developmental stages, and a well-defined and reproducible senescence program (Bleecker and Patterson, 1997). In many monocarpic plants, such as the pea and soybean, leaf senescence is coupled to development of the reproductive organ (Pic et al., 2002). However, mutations in Arabidopsis that caused male sterility, delayed flowering time, or early termination of the inflorescence have little effect on the timing of senescence in one particular leaf. Instead, the developmental age of the individual leaf is a major factor that governs leaf senescence (Hensel et al., 1993). The lack of correlative controls on leaf senescence in Arabidopsis leads to a more precise examination of the intrinsic process within a leaf that contributes to the observed age-related senescence. However, the reader is reminded that the findings in Arabidopsis may not reveal some of the molecular mechanisms underlying leaf senescence in other plants. Senescence is a complex process that integrates many other aspects of plant physiology, including leaf development and metabolism. A rich resource of well-characterized mutations in Arabidopsis is also beneficial, since some of these mutations can be utilized to understand the relationship between senescence and other plant physiology. Recognized for these points as a favorite model plant for senescence study, Arabidopsis has been productively utilized for identifying senescence regulators and for elucidating the regulatory mechanisms of leaf senescence through molecular and genetic approaches.

III Senescence Symptoms

Obvious visual symptoms of leaf senescence in Arabidopsis are loss of chlorophyll (degreening), desiccation, and eventual death. The events contributing...