Autophagy as a possible mechanism for micronutrient remobilization from leaves to seeds

Abstract

Seed formation is an important step of plant development which depends on nutrient allocation. Uptake from soil is an obvious source of nutrients which mainly occurs during vegetative stage. Because seed filling and leaf senescence are synchronized, subsequent mobilization of nutrients from vegetative organs also play an essential role in nutrient use efficiency, providing source-sink relationships. However, nutrient accumulation during the formation of seeds may be limited by their availability in source tissues. While several mechanisms contributing to make leaf macronutrients available were already described, little is known regarding micronutrients such as metals. Autophagy, which is involved in nutrient recycling, was already shown to play a critical role in nitrogen remobilization to seeds during leaf senescence. Because it is a non-specific mechanism, it could also control remobilization of metals. This article reviews actors and processes involved in metal remobilization with emphasis on autophagy and methodology to study metal fluxes inside the plant. A better understanding of metal remobilization is needed to improve metal use efficiency in the context of biofortification.

Keywords: Fe; Zn; atg; isotopic labeling; leaf senescence; nutrient fluxes; nutrient use efficiency; transition metal.

FIGURE 1

Uptake and remobilization pathways involved in seed filling with emphasis on source-sink relationships. Micronutrients from the rhizosphere (brown arrow) are taken up into roots and transported to the xylem vessels (shown in blue). After xylem loading, micronutrients are translocated into shoots for subsequent unloading. Micronutrients located in the xylem can also be unloaded into the xylem parenchyma of nodes to be transferred to phloem vessels (shown in red) by specific transporters (Sondergaard et al., 2004; Tanaka et al., 2008; Yamaji and Ma, 2009). This is essential for seed filling which is only achieved by the phloem sap (Patrick and Offler, 2001). Phloem micronutrients are unloaded to fill seeds. Because seed filling is also achieved by nutrient remobilized from senescent tissues (green arrow), seed formation requires close synchronization between sink formation and source organ senescence. Age, biotic and abiotic stresses contribute to orchestrate nutrient mobilization during leaf senescence with the formation of reproductive organs and seed filling (black arrows). Light and photoperiod act indirectly on leaf senescence by stimulating the development of the reproductive organs.

FIGURE 2

Sink/source transition at the cellular level. Active photosynthetic cells perform carbon fixation, energy production and anabolism and require micronutrients for these functions. Senescence modifies these sink cells into a source cells undergoing catabolism. Intense catabolism activities and nutrient recycling occurs in chloroplasts, cytosol, and vacuole allowing nutrient remobilization. Chloroplasts, which concentrate a large part of metals, are first affected (Zavaleta-Mancera et al., 1999). Pigment degradation directly takes place in chloroplasts (Hörtensteiner et al., 1995; Park et al., 2007). However, stromal proteins are degradated into the central vacuole through rubisco containing body (RCB: autophagosome) or into senescence associated vacuoles (SAV) through an ATG-independent route which is not well understand yet (Hörtensteiner and Feller, 2002; Ishida et al., 2008; Ishida et al., 2013). These dismantling mechanisms decrease chloroplast seize enabling whole chloroplast degradation via chlorophagy (Ishida et al., 2013). Peroxisomes are modified to glyoxysomes, which produce energy and soluble sugars from lipid catabolism (Buchanan-Wollaston, 1997; del Rìo et al., 1998). Mitochondria that remain intact until late after senescence onset, are in turn degraded when the energy demand decreases (Yoshida, 2003). Finally, membrane permeabilization causes loss of cytoplasm that finally leads to death. ROS, reactive oxygen species; SAV, senescence-associated vacuoles; RCB, rubisco containing body; N, nucleus.