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Ethylene-Orchestrated Circuitry Coordinates a Seedlingts Response

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Ethylene-Orchestrated Circuitry Coordinates a Seedlingts Response Ethylene-orchestrated circuitry coordinates INAUGURAL ARTICLE a seedling’s response to soil cover and etiolated growth Shangwei Zhonga,b, Hui Shia,b, Chang Xuea, Ning Weib,1, Hongwei Guoa,1, and Xing Wang Denga,b,1 aPeking–Yale Joint Center for Plant Molecular Genetics and Agro-biotechnology, National Key Laboratory of Protein and Plant Gene Research, and Peking–Tsinghua Center for Life Sciences, College of Life Sciences, Peking University, Beijing 100871, China; and bDepartment of Molecular, Cellular, and Developmental Biology, Yale University, New Haven, CT 06520 This contribution is part of the special series of Inaugural Articles by members of the National Academy of Sciences elected in 2013. Contributed by Xing Wang Deng, February 10, 2014 (sent for review January 2, 2014) The early life of terrestrial seed plants often starts under the soil in In the absence of light signals, the growth modulation of eti- subterranean darkness. Over time and through adaptation, plants olated seedlings is determined by the coaction of a variety of have evolved an elaborate etiolation process that enables seedlings plant hormones (12–16). For example, Gibberellin (GA) is to emerge from soil and acquire autotrophic ability. This process, known to promote hypocotyl elongation and repress photomor- however, requires seedlings to be able to sense the soil condition phogenic gene expression in darkness within the context of the and relay this information accordingly to modulate both the seed- etiolation program (17–19). The mechanism by which seedlings lings’ growth and the formation of photosynthetic apparatus. The monitor soil depth and texture, and modulate their growth pat- mechanism by which soil overlay drives morphogenetic changes in tern accordingly, however, remains poorly understood. Previous plants, however, remains poorly understood, particularly with research has suggested that ethylene gas is likely to play an im- regard to the means by which the cellular processes of different portant role in modulating plant growth and development, par- organs are coordinated in response to disparate soil conditions. ticularly in light of the fact that ethylene, as the smallest plant hormone, can rapidly spread throughout the plant (10, 20–26). Here, we illustrate that the soil overlay quantitatively activates PLANT BIOLOGY ’ – Ethylene is perceived by five receptors that are related to bac- seedlings ethylene production, and an EIN3/EIN3-like 1 dependent – ethylene-response cascade is required for seedlings to successfully terial two-component regulators (27 29), whereas the biological responses to ethylene are known to be mediated by ethylene emerge from the soil. Under soil, an ERF1 pathway is activated in – the hypocotyl to slow down cell elongation, whereas a PIF3 path- insensitive 3 and ethylene insensitive 3-like 1 (EIN3/EIL1) (30 33), two plant-specific transcription factors that are rapidly induced way is activated in the cotyledon to control the preassembly of by ethylene at the protein level (34–36). Loss of EIN3/EIL1 photosynthetic machinery. Moreover, this latter PIF3 pathway function has been known to lead to complete insensitivity to appears to be coupled to the ERF1-regulated upward-growth rate. ethylene (37, 38). In early physiological experiments, pea seed- The coupling of these two pathways facilitates the synchronized lings and bean roots have been shown to produce an increased progression of etioplast maturation and hypocotyl growth, which, amount of ethylene in response to mechanical stress (39, 40), in turn, ultimately enables seedlings to maintain the amount of whereas ethylene pathway mutants are found to exhibit defects in protochlorophyllide required for rapid acquisition of photoauto- their soil emergence capabilities (41). Moreover, ethylene has trophic capacity without suffering from photooxidative damage also been shown to induce dramatic morphological changes during the dark-to-light transition. Our findings illustrate the ex- known as “the triple response” on typical dark-grown seedlings istence of a genetic signaling pathway driving soil-induced plant (20, 38, 42). These changes include inhibition of hypocotyl and morphogenesis and define the specific role of ethylene in orches- root elongation, radial swelling (horizontal growth) of hypocotyl trating organ-specific soil responses in Arabidopsis seedlings. Significance plant hormone ethylene | chlorophyll biosynthesis | ROS | cell death Seedlings’ ability to both adapt to their soil environment and errestrial flowering plants often drop their seeds under soil or acquire photoautotrophic capacity under various buried con- Tlitter, which serves to protect the propagation process from ditions is a life-or-death issue for terrestrial flowering plants. hostile conditions such as cold temperatures and/or predators By designing and utilizing a standardized real-soil assay, we – (1 3). As a result of this soil cover and/or dense canopy, seeds identify the key features of germinating seedlings’ soil re- often germinate in subterranean darkness. Unlike seedlings that sponse and deduce that the gaseous phytohormone ethylene undergo germination in the light, which immediately undergo acts as the primary regulator of soil-induced plant morphoge- photomorphogenesis, seedlings that germinate under soil follow netic changes. Moreover, our study illustrates that an EIN3/ an adaptive growth program known as skotomorphogenesis or EIL1-conducted PIF3–ERF1 molecular circuitry enables seedlings etiolation (4–6). When seedlings finally emerge from soil, light to synchronize the rate of protochlorophyllide biosynthesis terminates the etiolation program and activates the conversion with upward growth, a mechanism critical to the prevention of of etioplasts to chloroplasts, which, in turn, enable the plants to photooxidative damage during seedlings’ initial transition gain photoautotrophic ability (7, 8). This transition from dark- from dark to light in natural conditions. ness to light is a point of particular vulnerability in the life cycle of a higher land plants, however, due to the fact that light energy Author contributions: S.Z., N.W., H.G., and X.W.D. designed research; S.Z., H.S., and C.X. performed research; S.Z., H.S., N.W., H.G., and X.W.D. analyzed data; and S.Z., H.S., absorbed by protochlorophyllide (Pchlide) (a precursor of chlo- N.W., H.G., and X.W.D. wrote the paper. rophyll) is extremely phototoxic and can potentially cause seedling The authors declare no conflict of interest. death by light-induced photooxidative damage (6, 9–11). To deal 1To whom correspondence may be addressed. E-mail: [email protected], ning. with these obstacles, higher land plants have adapted an elaborate [email protected], or [email protected]. etiolation program that allows for precise control of the progression This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. of etioplast development before their conversion into chloroplasts. 1073/pnas.1402491111/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1402491111 PNAS Early Edition | 1of8 Downloaded by guest on September 26, 2021 cells, and exaggeration of the apical hook (20, 43). This “triple response” seedling morphology is thought to optimize the seed- ling’s ability to push through the soil without damaging its shoot meristem. Nonetheless, little is known about the specific role of ethylene plays over the course of etiolation program under soil. Here, we demonstrate that the documented “triple response” is actually an adaptive response to soil overlay, and that ethylene is the primary mediator of plants’ soil response during growing out of soil. In soil-induced etiolation program, EIN3/EIL1 acts a point of convergence from which cellular activities of the cotyledon and hypocotyl are coordinated in accordance to the depth and texture of the soil in which a seedling finds itself. Once activated by the soil, EIN3/EIL1 stimulates ethylene response factor (ERF1) in the hypocotyl, which, in turn, inhibits cell elongation and slows down the upward-growth rate. Similarly, EIN3/EIL1 concurrently activates phytochrome-interacting fac- tor 3 (PIF3) in the cotyledon to repress Pchlide biosynthesis, and thus cope with the extended time in subterranean darkness. As a result of this synchronized mechanism, the progression of the Pchlide accumulation is optimized so as to ensure seedlings rapidly acquire photosynthetic capacity without experiencing photooxidative damage once they emerge from the soil. Fig. 1. Soil overlay quantitatively activates ethylene production and the endogenous level of EIN3 protein, which is essential for soil-induced mor- Results phogenetic changes in seedlings. (A) Ethylene production from 4-d-old dark Soil Overlay Quantitatively Activates Ethylene Production and EIN3 grown Col-0 seedlings on MS medium without soil covering (0 mm) or buried ± Protein Accumulation. To examine how Arabidopsis seedlings re- under soft soil (silicon powder) or firm soil (sand) of indicated depth. Mean spond to various buried conditions, we designed a set of conve- SD; n = 3. (B) Image analysis of 4-d-old dark grown EIN3p:EIN3-Luciferase/ nient and highly reproducible soil assays with which we ein3eil1 seedlings under white light (Left) or bioluminescence (Right). The monitored the emergence of seedlings from soil of divergent depth bioluminescence of EIN3p:EIN3-Luciferase/ein3eil1 indicates the EIN3 protein level. The seedlings were grown on MS medium without soil (No soil) or and texture (Fig. S1). We
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