Autophagy mediates grain yield and nitrogen stress resistance by modulating nitrogen remobilization in rice

Abstract

Autophagy, a conserved cellular process in eukaryotes, has evolved to a sophisticated process to dispose of intracellular constituents and plays important roles in plant development, metabolism, and efficient nutrients remobilization under suboptimal nutrients conditions. Here, we show that OsATG8b, an AUTOPHAGY-RELATED8 (ATG8) gene in rice, was highly induced by nitrogen (N) starvation. Elevated expression of OsATG8b significantly increased ATG8 lipidation, autophagic flux, and grain yield in rice under both sufficient and deficient N conditions. Overexpressing of OsATG8b could greatly increase the activities of enzymes related to N metabolism. Intriguingly, the 15N-labeling assay further revealed that more N was remobilized to seeds in OsATG8b-overexpressing rice, which significantly increased the N remobilization efficiency (NRE), N harvest index, N utilization efficiency (NUE), and N uptake efficiency (NUpE). Conversely, the osatg8b knock-out mutants had the opposite results on these characters. The substantial transcriptional changes of the overexpressed transgenic lines indicated the presence of complex signaling to developmental, metabolic process, and hormone, etc. Excitingly, the transgenic rice under different backgrounds all similarly be boosted in yield and NUE with OsATG8b overexpression. This work provides an excellent candidate gene for improving N remobilization, utilization, and yield in crops simultaneously.

Current Understanding of Leaf Senescence in Rice

“…The higher N remobilization efficiency of OsATG8b-overexpressors was demonstrated using 15 N labeling and tracing assays. On the contrary, the osatg8b knockout mutants showed the opposite phenotypes [110]. The specific roles of the different ATG8 isoforms in Arabidopsis and rice remain to be explored, as well as their respective involvement in nutrient recycling.…”

“…As the transcript levels of OsATG8a , OsATG8b , and OsATG8c are increased under N starvation, their overexpression was assayed in rice [ 107 , 108 , 109 , 110 ]. Irrespective of the OsATG8 isoforms, rice transformants display higher NUE and yield [ 107 , 108 , 109 , 110 ]. The OsATG8a -overexpressing lines accumulate more N in their grains and less in their dry remains compared to WT, which indicates a better N remobilization to the seeds that increase grain yield [ 107 ].…”

“…The OsATG8a -overexpressing lines accumulate more N in their grains and less in their dry remains compared to WT, which indicates a better N remobilization to the seeds that increase grain yield [ 107 ]. The overexpression of OsATG8b could improve NUE and increased grain yield by stimulating autophagy flux and by enhancing the activities of enzymes related to N metabolism [ 110 ]. The higher N remobilization efficiency of OsATG8b -overexpressors was demonstrated using 15 N labeling and tracing assays.…”

How Lipids Contribute to Autophagosome Biogenesis, a Critical Process in Plant Responses to Stresses

“…Accordingly, studies of plants overexpressing ATG genes support a beneficial impact of increasing autophagy activity which was associated with an enhanced resistance to drought [ 57 ], oxidative stress or necrotrophic pathogens [ 3 ]. Further, plants with higher constitutive autophagy exhibited delayed aging, and an enhanced plant growth and seed oil content suggesting better agronomical values (in both Arabidopsis [ 3 ] and rice [ 86 ]). Although this work opens the idea of manipulating autophagy activity as a way to increase crops tolerance to stress, at present, studies describing the effects of increasing or constitutively activating autophagy remains scarce.…”

Heterotrimeric G protein α subunit (GPA1) regulates the response to low-nitrogen stress in Arabidopsis by interacting with AtNRT1.4 and AtATG8a

“…Autophagy, a highly conserved mechanism that degrades and recycles intracellular materials to promote survival under different external environment stresses, exists extensively in animals and plants (Fan et al, 2020; Melino et al, 2021). In plants, autophagy plays a crucial role in nutrient recycling under conditions of nitrogen or carbon starvation (Chen et al, 2019; Zhen et al, 2019a; Zhen et al, 2019b; Zhen et al, 2021). Most autophagy-related genes (ATGs) are upregulated in response to nitrogen starvation, and in Arabidopsis , mutations in key autophagy-related genes, such as atg5, atg7, atg10 , and atg13a / atg13b , increase the sensitivity to low-nitrate stress, accelerate senescence, and enable the supply of sufficient nitrate (Zhao et al, 2019; Havé et al, 2019).…”