SummaryRecent applications of oxygen-sensitive microsensors have demonstrated steep oxygen gradients in developing seeds of various crops. Here, we present an overview on oxygen distribution, major determinants of the oxygen status in the developing seed and implications for seed physiology. The steady-state oxygen concentration in different seed tissues depends on developmental parameters, and is determined to a large extent by environmental factors. Photosynthetic activity of the seed significantly diminishes hypoxic constraints, and can even cause transient, local hyperoxia. Changes in oxygen availability cause rapid adjustments in mitochondrial respiration and global metabolism. We argue that nitric oxide (NO) is a key player in the oxygen balancing process in seeds, avoiding fermentation and anoxia in vivo. Molecular approaches aiming to increase oxygen availability within the seed are discussed.Abbreviations: At, Arabidopsis thaliana; AOX, alternative oxidase; COX, cytochrome C oxidase; HIF1, hypoxia-inducible factor; NO, nitric oxide; ROS, reactive oxygen species.
I. IntroductionThe modern atmosphere contains approx. 21 kPa oxygen. However, over the course of the past 550 million yr (Phanerozoic time), during which time the vascular plants invaded the land surface, plants have adapted to levels of atmospheric oxygen ranging from 13 to 51 kPa (Raven, 1991). This variation has been a major driver of plant evolution, and has led to the tuning New Phytologist (2009) 182: 17-30 doi: 10.1111/j. 1469-8137.2008.02752.x Key words: hypoxia, nitric oxide (NO), oxygen diffusion, oxygen sensing, seed development, seed photosynthesis, storage metabolism.
Tansley review Review 18New Phytologist ( of plant architecture/ultrastructure and metabolism to tolerate both low and high oxygen supply (Berner, 1999). Although over a shorter time-scale the atmospheric oxygen level may appear stable, plants must be able to adapt to variation in oxygen provision imposed by the local environment. For example, little oxygen is available to the plant root in a temporarily waterlogged soil, so plants have developed a number of strategies for acclimatization, avoidance and escape (Armstrong et al., 1994; Crawford & Brändle, 1996; Drew, 1997;Vartapetian et al., 2008). The diffusion of gas is 10 000 fold slower through a liquid medium than through air, so waterlogging rapidly leads to hypoxic and eventually even to anoxic conditions. Under hypoxia, the concentration of oxygen limits mitochondrial ATP production (oxidative phosphorylation), whereas under anoxia there is essentially no oxygen available for mitochondrial respiration. A restricted capacity for oxygen diffusion, in conjunction with a high rate of cellular metabolism, can generate hypoxia even in aerial organs such as the fruit (Ke et al., 1995), certain vascular tissues (Kimmers & Stringer, 1988), the pollen grain (Leprince & Hoekstra, 1998) and the seed (Rolletschek et al., 2002). From a historical perspective, seed germination and subsequent seedling growth has been one of...