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Brief ReportIN BRIEF
Open Access

Life’s a Gas under Pressure: Ethylene and Etioplast Maintenance in Germinating Seedlings

Patrice A. Salomé
Patrice A. Salomé
Department of Chemistry and BiochemistryUniversity of California, Los Angeles
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Published December 2017. DOI: https://doi.org/10.1105/tpc.17.00939

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  • © 2017 American Society of Plant Biologists. All rights reserved.

Seedlings that emerge from the soil at the beginning of spring are true survivors: They found a pocket of water for hydration, escaped pecking birds and human footsteps, and wound their way up through rough particles to the soil surface without being reduced to shreds. This latter feat comes in large part from adaptations in growth patterns of etiolated seedlings (grown in the dark): elongated hypocotyls, unexpanded and unopened cotyledons, and a pronounced apical hook that presents the least amount of resistance to the soil medium while protecting the apical meristem until soil emergence. In these underground seedlings, chloroplast development is arrested at the etioplast stage; future photosynthetic membranes organize into a highly regular structure called the prolamellar body to sequester the chlorophyll precursor protochlorophyllid and minimize photooxidative damage upon light exposure.

The transcription factor PHYTOCHROME INTERACTING FACTOR3 (PIF3) is essential for this process, as it represses light-mediated development in the dark. As seedlings come closer to the soil surface and receive more light, PIF3 protein levels gradually decrease to allow seedling greening (Shi et al., 2016). But PIF3 is not the only player in this game: Germinating seedlings also measure the depth of soil they are buried under via the transcription factor ETHYLENE INSENSITIVE3 (EIN3) (Zhong et al., 2014). Etiolated seedlings pushing through soil produce the gaseous hormone ethylene as a response to physical impedance (Goeschl et al., 1966). Ethylene prevents the degradation of EIN3 and results in the classic “triple-response”: short and fat hypocotyls and a pronounced apical hook. As seedlings grow closer to the surface, soil pressure lessens, ethylene production decreases, and EIN3 protein degradation accelerates (Shi et al., 2016). Now, new results by Liu et al. (2017) show how PIF3 and EIN3 cooperate at the molecular and transcriptional level to suppress the maturation of etioplasts into chloroplasts until seedlings emerge from underneath the soil.

Functional overlap between PIF3 and EIN3 first emerges from gene expression profiles of etiolated seedlings. Over half of the genes normally repressed in the dark by EIN3 and EIL1 (a related protein) are also induced by red light through PIF3. The explanation? EIN3 and PIF3 proteins physically interact, bind largely to the same elements within target promoters, and influence each other’s binding affinity without affecting each other’s stability. The authors also show that the expression of most genes encoding the core photosynthetic machinery, including light-harvesting complex proteins (LHCAs and LHCBs) and chlorophyll biosynthesis enzymes, is induced in etiolated pif3 single and ein3 eil1 double mutants.

This premature expression of chloroplast building blocks in etiolated seedlings comes at a cost. Photosynthetic membranes in pif3 and ein3 eil1 etioplasts start to organize in prothylakoid membranes and lose the highly regular arrangement of the prolamellar body. Overexpression of PIF3 (in ein3 eil1) or EIN3 (in pif3) does not rescue full prolamellar body formation and the pif3 ein3 eil1 triple mutant shows the same extent of prothylakoid membranes as the pif3 single and ein3 eil1 double mutants. Both of these results underscore the true synergy between PIF3 and EIN3 (Liu et al., 2017).

What does it take to nudge the prolamellar body to reorganize into prothylakoid membranes? Apparently, not much: Overexpression of individual members of the LHCB family results in extensive unraveling of the prolamellar body in etioplasts (Liu et al., 2017). These lines still accumulate protochlorophyllid, but the absence of the prolamellar body for sequestration of the chlorophyll precursor now renders seedlings highly sensitive to photooxidation when exposed to light (see figure), just like in pif3 and ein3 eil1 mutants.

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Premature chloroplast development causes photooxidative damage. Seedlings were grown in the dark before transfer to white light. Seedling greening was obvious only in Col-0 from chlorophyll autofluorescence, while ein3 eil1 and Lhcb2.1 ox lines showed extensive reactive oxygen species accumulation due to loss of prolamellar body (as shown in etioplast transmission electron microscopy). (Adapted from Liu et al. [2017], Figures 2, 7, and 8.)

So what have I learned today? I’ve learned that PIF3 and EIN3 act together in etiolated seedlings to rein in chloroplast development before soil emergence, with PIF3 sensing light filtering through the soil, and EIN3 measuring soil depth and that the triple response, famously exploited for the isolation of ethylene mutants, is actually a seedling’s natural response to soil pressure. What we still don’t know, but promises to turn on the pressure on ethylene research, is how the weight of soil above etiolated seedlings activates ethylene production.

Footnotes

  • www.plantcell.org/cgi/doi/10.1105/tpc.17.00939

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References

  1. ↵
    1. Goeschl, J.D.,
    2. Rappaport, L.,
    3. Pratt, H.K.
    (1966). Ethylene as a factor regulating the growth of pea epicotyls subjected to physical stress. Plant Physiol. 41: 877–884.
    OpenUrlAbstract/FREE Full Text
  2. ↵
    1. Liu, X.,
    2. Liu, R.,
    3. Li, Y.,
    4. Shen, X.,
    5. Zhong, S.,
    6. Shi, H.
    (2017). EIN3 and PIF3 form an interdependent module that represses chloroplast development in buried seedlings. Plant Cell 29: 3051–3067.
    OpenUrlAbstract/FREE Full Text
  3. ↵
    1. Shi, H.,
    2. Liu, R.,
    3. Xue, C.,
    4. Shen, X.,
    5. Wei, N.,
    6. Deng, X.W.,
    7. Zhong, S.
    (2016). Seedlings transduce the depth and mechanical pressure of covering soil using COP1 and ethylene to regulate EBF1/EBF2 for soil emergence. Curr. Biol. 26: 139–149.
    OpenUrl
  4. ↵
    1. Zhong, S.,
    2. Shi, H.,
    3. Xue, C.,
    4. Wei, N.,
    5. Guo, H.,
    6. Deng, X.W.
    (2014). Ethylene-orchestrated circuitry coordinates a seedling’s response to soil cover and etiolated growth. Proc. Natl. Acad. Sci. USA 111: 3913–3920.
    OpenUrlAbstract/FREE Full Text
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Life’s a Gas under Pressure: Ethylene and Etioplast Maintenance in Germinating Seedlings
Patrice A. Salomé
The Plant Cell Dec 2017, 29 (12) 2951-2952; DOI: 10.1105/tpc.17.00939

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Life’s a Gas under Pressure: Ethylene and Etioplast Maintenance in Germinating Seedlings
Patrice A. Salomé
The Plant Cell Dec 2017, 29 (12) 2951-2952; DOI: 10.1105/tpc.17.00939
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The Plant Cell: 29 (12)
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Vol. 29, Issue 12
Dec 2017
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