A comprehensive, genome-wide analysis of autophagy-related genes identified in tobacco suggests a central role of autophagy in plant response to various environmental cues

Abstract

Autophagy is an evolutionarily conserved mechanism in both animals and plants, which has been shown to be involved in various essential developmental processes in plants. Nicotiana tabacum is considered to be an ideal model plant and has been widely used for the study of the roles of autophagy in the processes of plant development and in the response to various stresses. However, only a few autophagy-related genes (ATGs) have been identified in tobacco up to now. Here, we identified 30 ATGs belonging to 16 different groups in tobacco through a genome-wide survey. Comprehensive expression profile analysis reveals an abroad expression pattern of these ATGs, which could be detected in all tissues tested under normal growth conditions. Our series tests further reveal that majority of ATGs are sensitive and responsive to different stresses including nutrient starvation, plant hormones, heavy metal and other abiotic stresses, suggesting a central role of autophagy, likely as an effector, in plant response to various environmental cues. This work offers a detailed survey of all ATGs in tobacco and also suggests manifold functions of autophagy in both normal plant growth and plant response to environmental stresses.

Comprehensive Analysis of Autophagy-Related Genes in Sweet Orange (Citrus sinensis) Highlights Their Roles in Response to Abiotic Stresses

“…The quantity of ATGs in sweet orange is similar to the quantity in grape (35 VvATGs) [13], banana (32 MaATGs) [12], rice (33 OsATGs) [7], and foxtail millet (37 SiATGs) [11], suggesting very conservative evolution of ATGs in these plants. Among the 19 core CsATGs, we found that CsATG1, CsATG8, and CsATG18 contained multiple members, which is similar to that in Arabidopsis and other plants [1,8,13]. However, unlike having two ATG4, ATG12, and ATG13 genes and one VTI12 in Arabidopsis, sweet orange has one member of CsATG4, CsATG12, and CsATG13 and four members of CsVTI12.…”

“…However, unlike having two ATG4, ATG12, and ATG13 genes and one VTI12 in Arabidopsis, sweet orange has one member of CsATG4, CsATG12, and CsATG13 and four members of CsVTI12. This indicates a citrus crop-specificity in the number of these ATGs [1,8]. On the basis of gene duplication analysis, a high proportion of segmental duplications was predicted for those multiple members of CsATGs, especially for CsATG8.…”

“…The first ATG gene was identified from yeast, and at least 32 ATGs have been shown to participate in yeast autophagy [5,6]. To date, many homologues of ATGs have been identified from various plant species, including 40 AtATGs in Arabidopsis [1,3] (Arabidopsis thaliana, At), 33 OsATGs in rice [7] (Oryza sativa, Os), 30 NtATGs in tobacco [8] (Nicotiana tabacum, Nt), 45 ZmATGs in maize [9] (Zea mays, Zm), 29 CaATGs in pepper [10] (Capsicum annuum, Ca), 37 SiATGs in foxtail millet [11] (Setaria italic, Si), 32 MaATGs in banana [12] (Musa acuminate, Ma), and 35 VvATGs in grapevine [13] (Vitis vinifera, Vv). According to the reported characterizations of ATGs in yeast and Arabidopsis, these ATGs can be divided into the following functional groups: (1) the ATG1/13 kinase complex consisting of ATG1, ATG13, ATG20, and TOR (target of rapamycin kinase), mainly functioning on autophagy induction and initiation; (2) the PI3K (phosphatidylinositol 3 kinase) complex consisting of ATG6, VPS15 (vacuolar protein sorting-associated protein), and VPS34 that is involved in vesicle nucleation and autophagosome formation; (3) the ATG9/2/18 complex consisting of ATG9, ATG2, and ATG18 that is responsible for the delivery of membranes for autophagosome formation; (4) the ubiquitin-like ATG8-PE (phosphatidylethanolamine) conjugation pathway (including ATG3, ATG4, ATG7, and ATG8) and ATG12-ATG5 conjugation pathway (including ATG5, ATG7, ATG10, ATG12, and ATG16) that are involved in the elongation of autophagic vesicles; and (5) the VTI12 (vesicle transport v-soluble N-ethylmaleimide-sensitive-factor attachment protein receptor (SNARE) protein) family belonging to the SNARE group, which contributes to the fusion of autophagosomes with vacuoles [1][2][3][4]6].…”

Boosting autophagy in sexual reproduction: a plant perspective

“…By contrast, the expression levels of some ATG s are low, such as in flowers, shoot apex and roots, possibly due to their different functional specificity in various types of plant tissues and cells. Similarly, in Nicotiana tabacum , the expression levels of some NtATG s are also particularly high in pollen and anthers (Zhou et al , ). These data may suggest potential regulatory roles of autophagy in proper development and/or functions of male gametes.…”

Autophagy: An Important Biological Process That Protects Plants from Stressful Environments

“…Thus far, over 30 ATG s have been identified in Arabidopsis , rice, tobacco, and pepper based on comprehensive, genome-wide analysis (Xia et al, 2011; Zhou et al, 2015; Zhai et al, 2016). ATGs can be divided into three categories with respect to their function: (i) ATG1-ATG13 comprising the kinase complex, an upstream regulator that initiates autophagosome formation (Suttangkakul et al, 2011); (ii) The ATG9 and ATG6/vps30 complexes involved in vacuolar protein sorting in which ATG9 interacts with ATG2 and ATG18, boosting phagophore expansion.…”