Autophagy in sexual plant reproduction as an emerging field

Abstract

Autophagy is an evolutionary conserved system for clearing and recycling cellular components. Critical roles of autophagy in the responses of plant to different environmental stresses have been revealed during past decades. However, little is known about the role of autophagy in plant developmental processes, especially in the processes of sexual plant reproduction. Here, we briefly discuss recent advances in the emerging field and wish to bring some potential research directions into attention. Possible divergence of molecular mechanism of autophagy in respect to the current debatable view is also discussed.

Autophagy is an evolutionary conserved mechanism for eliminating damaged or unwanted materials and recycling nutrients during environmental stresses and normal developmental processes.¹ Remarkable progresses have been made in understanding of the morphologic characteristics, physiological roles and canonical regulatory pathways of autophagy in yeasts and animals.^2-4 However, little is known about plant autophagy, especially, about its biological impact and underlying molecular mechanism although plant scientists have made great efforts in this field and have made it to be one of the most energetic fields in plant science during past decades.

Previously, numerous studies in the field of plant autophagy implied that autophagy may work as central effector in plant responses to various environmental cues such as nutrient starvation, oxidative stress, drought, salt and other abiotic stresses for plant adaptation in different severe conditions.^5-8 Whereas, less attention has been paid on the roles of plant autophagy in normal developmental processes. There are only a few examples indicating that plant autophagy are also acting in leaf starch degeneration,⁹ tracheary element differentiation,¹⁰ senescence^11,12 and life span extension.¹³

Recently, critical roles of plant autophagy during sexual plant reproduction have been revealed in 2 transient cell models, tapetum cells of Oryza sativa¹⁴ and suspensor cells of Picea abies,¹⁵ respectively. In O. sativa, OsATG7 was found to be essential for lipid metabolism and male fertility. Autophagosome-like structures were observed in tapetum cells surrounding microspores in wild type anthers, but no visible autophagosome-like structures was found in the sterile Osatg7 knockout mutants, suggesting that autophagy in tapetum cells are likely required for male reproductive development.¹⁴ In P. abies, autophagy has been reported to be necessary for vacuolar cell death of suspensor cell, which is essential for normal embryogenesis. Silencing of ATG5 or ATG6 leads to autophagy deficiency, resulting in abrogation of suspensor formation and consequent embryo development.¹⁵ These 2 examples implied that plant autophagy not only functions in stress conditions, but also in different plant developmental processes in normal condition, especially in vacuolar cell death of transient cells. The vacuolar cell death is believed to be ubiquitously presented in the processes of sexual plant reproduction e.g. nonfunctional megaspores degeneration, synergid cell death and programmed cell death of suspensor. In addition, our recent work also suggests manifold functions of autophagy in normal plant growth. The interesting expression patterns of ATGs imply their unique roles in some critical stages of sexual plant reproduction, such as gametophyte development, gametogenesis and embryogenesis.⁷ These novel findings indicate an emerging field of autophagy in sexual plant reproduction. Although it is known that timely elimination of the temporary cells is critical for plant fertility during sexual plant reproduction, how the plant autophagy plays its role in these processes and how it links to vacuolar cell death of transient cells are still the questions with great interesting for further study.

However, one of major problem is that no visible developmental defects can be found in knockout mutants of tested ATG genes (Autophagy related genes) in Arabidopsis thaliana under normal nutrient-rich conditions. Thus, if autophagy indeed plays a critical role in plant development seems questionable. In our opinion, it is still too early to make any conclusion about this aspect. In fact, our early expression profile analysis of ATGs in tobacco has revealed some distinct characteristics of ATG expression at least in the process of sexual plant reproduction compared with that in A. thaliana and O. sativa.⁷ Roles and functions of plant ATGs in autophagy may vary in different plant species. It should be a worthy work for exploring and comparing the roles of autophagy in plant development, especially in the process of sexual plant reproduction, among different model plants to get a more reliable survey of the plant autophagy. In addition, almost all known plant ATGs were found according to the clues from animal. The most common method used to identify molecular components regulating plant autophagy is to identify the homologues of ATGs in yeast and mammalian. Indeed, most ATG homologues have been identified in A. thaliana, N. tabacum and O. sativa, respectively. However, one possibility has been largely neglected, that is, plant may have some plant-specific autophagy pathways established during evolution. These pathways, if any, are impossible to be found by current techniques. In fact, no homologues of ATG14, ATG17, ATG23 and ATG27 have been identified in plant, and several ATG homologues in plants have multiple isoforms with functional divergence, which differ from that in yeast and mammalians. Furthermore, the research about plant autophagy, especially about its molecular pathways, is still in its infancy and the precise functions of these ATG homologues in autophagy are still largely unknown. Some of them may be critical for plant development. Recently, cytosolic glyceraldehyde-3-phosphate dehydrogenases (GAPCs) have been reported to negatively regulate autophagy through the interaction with ATG3, suggesting other proteins except ATGs are also involved in the regulation of plant autophagy.¹⁶ All these data indicate that we have tremendous work to do before making any conclusion about the role of autophagy in plant development.

Although no clear picture about plant autophagy could be drawn from our current knowledge, recent findings mentioned above have provided our new insights into the novel roles of autophagy in the developmental processes and molecular mechanism underlying plant autophagy. These works also raise many basic questions worthy to be answered in the further studies. For example, what are the conservation and divergence of autophagy between plants and mammalians? What are the plant specific molecular mechanism regulating autophagy and its conservation among different plant species? What are the key molecular components linking plant autophagy and vacuolar cell death? What are the roles of autophagy in the processes of sexual plant reproduction, especially in the alternation of generations, in the selective inherit of cytoplasm of gametes, and in embryonic cell fate specification? To addressing these questions will surely update our understanding of plant autophagy and help us to discover more details of the molecular mechanisms of the plant autophagy.

Disclosure of Potential Conflicts of Interest

No potential conflicts of interest were disclosed.

Funding

This project was supported by National Natural Science Foundation of China (31400171) and China Postdoctoral Science Foundation (2015M570663).