Skip to main content

Main menu

  • Home
  • Content
    • Current Issue
    • Archive
    • Preview Papers
  • About
    • Editorial Board and Staff
    • About the Journal
    • Terms & Privacy
  • More
    • Alerts
    • Contact Us
  • Submit a Manuscript
    • Instructions for Authors
    • Submit a Manuscript
  • Other Publications
    • Plant Physiology
    • The Plant Cell
    • Plant Direct
    • The Arabidopsis Book
    • Teaching Tools in Plant Biology
    • ASPB
    • Plantae

User menu

  • My alerts
  • Log in

Search

  • Advanced search
Plant Cell
  • Other Publications
    • Plant Physiology
    • The Plant Cell
    • Plant Direct
    • The Arabidopsis Book
    • Teaching Tools in Plant Biology
    • ASPB
    • Plantae
  • My alerts
  • Log in
Plant Cell

Advanced Search

  • Home
  • Content
    • Current Issue
    • Archive
    • Preview Papers
  • About
    • Editorial Board and Staff
    • About the Journal
    • Terms & Privacy
  • More
    • Alerts
    • Contact Us
  • Submit a Manuscript
    • Instructions for Authors
    • Submit a Manuscript
  • Follow PlantCell on Twitter
  • Visit PlantCell on Facebook
  • Visit Plantae
In BriefIN BRIEF
Open Access

How to Eat One’s Feelings: Autophagy and Phosphatidylinositol 3-Phosphate

Patrice A. Salomé
Patrice A. Salomé
Science Editor
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Patrice A. Salomé

Published December 2020. DOI: https://doi.org/10.1105/tpc.20.00870

  • Article
  • Figures & Data
  • Info & Metrics
  • PDF
Loading
  • © 2020 American Society of Plant Biologists. All rights reserved.

Moving around taught me two essential skills, only one being relevant here: how to put up wallpaper, and how critical it is to label boxes to help the moving company drop them at their intended location. Now think of a cell: the boxes are vesicles, their contents are proteins and metabolites, and the starting location and final destination of these vesicles will depend on the type of protein/metabolite and the growth environment. Like any good packing champion, plant cells label their assortment of vesicles, not with a Sharpie but with phospholipids like phosphatidylinositol 3-phosphate (PI3P) to dictate their intended destination(s). The decoration of vesicles with PI3P is especially important during autophagy, whereby cells recycle proteins and their trapped amino acids through trafficking to the vacuole (Noack and Jaillais, 2017).

The biosynthesis of PI3P relies on PI3 kinases (PI3Ks), for which plants are thought to employ a single protein complex catalyzing its biosynthesis. In Arabidopsis (Arabidopsis thaliana), the single PI3K VACUOLAR PROTEIN SORTING34 (VPS34) forms a complex with three accessory proteins: VPS15, AUTOPHAGY-RELATED6 (ATG6), and either ATG14 or VPS38. As might be expected, disrupting PI3P biosynthesis spells trouble for the proper delivery of cargo within the cell. Unfortunately, single loss-of-function mutations in VPS34, VPS15, or ATG6 cannot be maintained in the homozygous state in Arabidopsis, underscoring the critical importance of PI3P but making a genetic dissection very challenging.

In their recent article, Fen Liu and colleagues (Liu et al., 2018) turned to the remaining subunit of the complex, which is filled either by ATG14 or VPS38. The authors hypothesized that loss of function in ATG14 (encoded by two genes in Arabidopsis: ATG14a and ATG14b) would result in milder phenotypes and allow a genetic analysis. The vps38 mutants had been previously shown to be viable but were characterized by smaller rosettes with twisted leaves, along with alterations in endosomal sorting (Lee et al., 2018; Liu et al. 2018). By contrast, double mutants inactivating both ATG14 copies, generated via genome editing, exhibited normal leaves and rosettes, indicating that ATG14 is not essential. However, a closer inspection showed a clear disruption of autophagic transport, establishing that ATG14 and VPS38 have non-redundant functions in the PI3K complex. Like other components of the autophagic machinery, the authors then showed that ATG14 associates with autophagic vesicles that are themselves imported into vacuoles.

Surprisingly, the expected prediction that atg14a atg14b vps38 triple mutant plants would be non-viable, just like mutants eliminating the other three PI3K components, turned out to be false, as the authors were able to find viable triple mutant plants, although at lower frequencies than anticipated (see figure). The existence of the triple mutant raised an obvious question: Do ATG14 and VPS38 even affect PI3P synthesis? The answer was “yes,” but not completely. From arduous phospholipid assays, only a 50% reduction in PI3P levels was seen in the triple mutant, suggesting that the PI3K VPS34 may work without this fourth subunit, or that plants utilize another yet to be discovered PI3K component. To specifically address this point, the authors relied on the inhibitor wortmannin, which is specific to VPS34. Although wild-type Arabidopsis seedlings showed a mild growth suppression when exposed to low concentrations of wortmannin, the triple mutant was severely compromised, suggesting that the VPS34-containing PI3K is likely the sole source of PI3P in Arabidopsis.

Figure1
  • Download figure
  • Open in new tab
  • Download powerpoint

atg14a atg14b Genetically Interacts with vps38.

Representative leaves from 5-week old plants grown in long days (16 h light:8 h dark) for the wild type (Col-0) and various mutants in the PI3P biosynthesis complex. Note the genetic interaction between atg14a atg14b and vps38-1, as evidenced by smaller and more twisted leaves.

(Adapted from Liu et al. [2020], Figure 8.)

As a geneticist, discovering that your favorite gene is essential is both rewarding and disappointing because the associated phenotypes are rather dull and technically challenging to work around. With this work, Liu et al. (2018) describe a complement of single, double, and triple mutants altering function in non-essential subunits of the PI3K complex to reveal the essential functions of the whole complex. Combined with chemical inhibition of PI3P biosynthesis, the results described here provide the foundation for a meticulous dissection of PI3P biology at the biochemical, cellular, and physiological levels.

Footnotes

  • www.plantcell.org/cgi/doi/10.1105/tpc.20.00870

  • ↵[OPEN] Articles can be viewed without a subscription.

References

  1. ↵
    1. Lee, H.N.,
    2. Zarza, X.,
    3. Kim, J.H.,
    4. Yoon, M.J.,
    5. Kim, S.-H.,
    6. Lee, J.-H.,
    7. Paris, N.,
    8. Munnik, T.,
    9. Otegui, M.S.,
    10. Chung, T.
    (2018). Vacuolar trafficking protein VPS38 is dispensable for autophagy. Plant Physiol. 176: 1559–1572.
    OpenUrlAbstract/FREE Full Text
  2. ↵
    1. Liu, F.,
    2. Hu, W.,
    3. Li, F.,
    4. Marshall, R.S.,
    5. Zarza, X.,
    6. Munnik, T,
    7. Vierstra, R.D.
    (2020). AUTOPHAGY-RELATED14 and its associated phosphatidylinositol 3-kinase complex promotes autophagy in Arabidopsis. Plant Cell 32: 3939–3960.
    OpenUrlAbstract/FREE Full Text
  3. ↵
    1. Liu, F.,
    2. Hu, W.,
    3. Vierstra, R.D.
    (2018). The vacuolar protein sorting-38 subunit of the Arabidopsis phosphatidylinositol-3-kinase complex plays critical roles in autophagy, endosome sorting, and gravitropism. Front Plant Sci 9: 781.
    OpenUrl
  4. ↵
    1. Noack, L.C.,
    2. Jaillais, Y.
    (2017). Precision targeting by phosphoinositides: How PIs direct endomembrane trafficking in plants. Curr. Opin. Plant Biol. 40: 22–33.
    OpenUrl
PreviousNext
Back to top

Table of Contents

Print
Download PDF
Email Article

Thank you for your interest in spreading the word on Plant Cell.

NOTE: We only request your email address so that the person you are recommending the page to knows that you wanted them to see it, and that it is not junk mail. We do not capture any email address.

Enter multiple addresses on separate lines or separate them with commas.
How to Eat One’s Feelings: Autophagy and Phosphatidylinositol 3-Phosphate
(Your Name) has sent you a message from Plant Cell
(Your Name) thought you would like to see the Plant Cell web site.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Citation Tools
How to Eat One’s Feelings: Autophagy and Phosphatidylinositol 3-Phosphate
Patrice A. Salomé
The Plant Cell Dec 2020, 32 (12) 3656-3657; DOI: 10.1105/tpc.20.00870

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Request Permissions
Share
How to Eat One’s Feelings: Autophagy and Phosphatidylinositol 3-Phosphate
Patrice A. Salomé
The Plant Cell Dec 2020, 32 (12) 3656-3657; DOI: 10.1105/tpc.20.00870
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
  • Tweet Widget
  • Facebook Like
  • Google Plus One

Jump to section

  • Article
    • Footnotes
    • References
  • Figures & Data
  • Info & Metrics
  • PDF

In this issue

The Plant Cell: 32 (12)
The Plant Cell
Vol. 32, Issue 12
Dec 2020
  • Table of Contents
  • Table of Contents (PDF)
  • Cover (PDF)
  • About the Cover
  • Index by author
View this article with LENS

More in this TOC Section

  • Got Rosettes? Phenotype Them Fast, Accurately, and Easily with ARADEEPOPSIS!
  • Ripe for the Picking: Finding the Gene Behind Variation in Strawberry Fruit Color
  • Hold Me, Fold Me...or Not!
Show more IN BRIEF

Similar Articles

Our Content

  • Home
  • Current Issue
  • Plant Cell Preview
  • Archive
  • Teaching Tools in Plant Biology
  • Plant Physiology
  • Plant Direct
  • Plantae
  • ASPB

For Authors

  • Instructions
  • Submit a Manuscript
  • Editorial Board and Staff
  • Policies
  • Recognizing our Authors

For Reviewers

  • Instructions
  • Peer Review Reports
  • Journal Miles
  • Transfer of reviews to Plant Direct
  • Policies

Other Services

  • Permissions
  • Librarian resources
  • Advertise in our journals
  • Alerts
  • RSS Feeds
  • Contact Us

Copyright © 2021 by The American Society of Plant Biologists

Powered by HighWire