Embryonic photosynthesis affects post-germination plant growth Ayala Sela, Urszula Piskurewicz, Christian Megies, Laurent Mène-Saffrané, Giovanni Finazzi, Luis Lopez-Molina To cite this version: Ayala Sela, Urszula Piskurewicz, Christian Megies, Laurent Mène-Saffrané, Giovanni Finazzi, et al.. Embryonic photosynthesis affects post-germination plant growth. Plant Physiology, American Society of Plant Biologists, 2020, 182 (4), pp.2166-2181. 10.1104/pp.20.00043. hal-02526415 HAL Id: hal-02526415 https://hal.archives-ouvertes.fr/hal-02526415 Submitted on 9 Oct 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. 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Distributed under a Creative Commons Attribution| 4.0 International License Embryonic Photosynthesis Affects Post-Germination Plant Growth1[OPEN] Ayala Sela,a Urszula Piskurewicz,a Christian Megies,a Laurent Mène-Saffrané,b Giovanni Finazzi,c and Luis Lopez-Molinaa,d,2,3 aDepartment of Botany and Plant Biology, University of Geneva, 1211 Geneva, Switzerland bDepartment of Biology, University of Fribourg, 1700 Fribourg, Switzerland cUniversité Grenoble Alpes, Centre National de la Recherche Scientifique, Commissariat à l’Énergie Atomique et aux Énergies Alternatives, Institut National de la Recherche Agronomique, Interdisciplinary Research Institute of Grenoble - Cell & Plant Physiology Laboratory, 38000 Grenoble, France dInstitute of Genetics and Genomics in Geneva, University of Geneva, 1211 Geneva, Switzerland ORCID IDs: 0000-0002-9523-9123 (U.P.); 0000-0003-0463-1187 (L.L.-M.). Photosynthesis is the fundamental process fueling plant vegetative growth and development. The progeny of plants relies on maternal photosynthesis, via food reserves in the seed, to supply the necessary energy for seed germination and early seedling establishment. Intriguingly, before seed maturation, Arabidopsis (Arabidopsis thaliana) embryos are also photosynthetically active, the biological significance of which remains poorly understood. Investigating this system is genetically challenging because mutations perturbing photosynthesis are expected to affect both embryonic and vegetative tissues. Here, we isolated a temperature-sensitive mutation affecting CPN60a2, which encodes a subunit of the chloroplast chaperonin complex CPN60. When exposed to cold temperatures, cpn60a2 mutants accumulate less chlorophyll in newly produced tissues, thus allowing the specific disturbance of embryonic photosynthesis. Analyses of cpn60a2 mutants were combined with independent genetic and pharmacological approaches to show that embryonic photosynthetic activity is necessary for normal skoto- and photomorphogenesis in juvenile seedlings as well as long-term adult plant development. Our results reveal the importance of embryonic photosynthetic activity for normal adult plant growth, development, and health. Seed development in Arabidopsis (Arabidopsis thali- and walking-stick, during which the basic architecture ana) is initiated after a double fertilization event, char- of the plant embryo is established following a pattern acteristic of flowering plants, which produces the organized along an apical-basal and radial axis (ten endosperm and the zygote. Seed development can be Hove et al., 2015). Eventually, 8–10 d after fertiliza- divided in two phases. The first phase is that of em- tion, this first phase ends with the cessation of cell di- bryogenesis per se, i.e. the zygote undergoes morpho- vision and the formation of the plant embryo, at which genesis through several rounds of cell division and stage the embryo is surrounded by a single cell layer of differentiation. This consists of successive develop- endosperm. Thereupon, the second phase, or seed mental stages, referred to as globular, heart, torpedo, maturation phase, is initiated, whereby embryonic cells expand as a result of protein and lipid food reserve 1 accumulation. Acquisition of osmotolerance and seed This work was supported by the Swiss National Science Founda- desiccation is also an important characteristic of seed tion (grant nos. 31003A-152660/1 and 31003A-179472/1), the State of maturation (Leprince et al., 2017). Eventually, the Geneva, the French National Research Agency, Grenoble Alliance for Integrated Structural Cell Biology (grant no. ANR-10-13 LABEX-04 maturation phase produces a highly resistant and food- GRAL Labex to G.F.), and the Interdisciplinary Research Institute of rich embryo, which remains surrounded by a single cell Grenoble. layer of mature endosperm. In the mature seed, the 2Author for contact: [email protected]. living endosperm and embryo tissues are shielded by a 3Senior author. protective external layer of dead maternal coat, namely The author responsible for distribution of materials integral to the the testa, consisting of differentiated and tannin-rich findings presented in this article in accordance with the policy de- integumental ovular tissues. Hence, seed develop- scribed in the Instructions for Authors (www.plantphysiol.org) is: ment produces a desiccated, metabolically inert, and Luis Lopez-Molina ([email protected]). highly resistant plant embryo that possesses energetic A.S. and L.L.-M. conceptualized and designed experiments, and autonomy needed to fuel its germination and early wrote the article; A.S. performed the experiments; U.P. performed the immunoblot experiments; A.S. and G.F. performed and analyzed the seedling establishment. electrochromic shift experiments; C.M. performed map-based clon- Photosynthesis is the fundamental process occurring ing; L.M.-S. performed fatty acid methyl ester quantification. in plant chloroplasts allowing plants to convert solar en- [OPEN]Articles can be viewed without a subscription. ergy into chemical energy, which fuels their growth and www.plantphysiol.org/cgi/doi/10.1104/pp.20.00043 development (Johnson, 2016). During embryogenesis, the 2166 Plant PhysiologyÒ, April 2020, Vol. 182, pp. 2166–2181, www.plantphysiol.org Ó 2020 American Society of Plant Biologists. All Rights Reserved. Downloaded from on May 12, 2020 - Published by www.plantphysiol.org Copyright © 2020 American Society of Plant Biologists. All rights reserved. Embryonic Photosynthesis Primes Plant Growth Arabidopsis embryo, as well as that of other oilseed receptor TOC159, germinate normally but exhibit plants, is green and photosynthetically active (Borisjuk seedling lethality due to their inability to produce and Rolletschek, 2009; Puthur et al., 2013; Allorent et al., functional chloroplasts (Tada et al., 2014; Pogson et al., 2015). The photosynthetic phase of the embryo starts early 2015). Yet, the developing embryo invests in what upon embryogenesis, at the globular stage, when plastids could be regarded as a high energy-consuming pro- differentiate into mature chloroplasts and chlorophyll cess of manufacturing and disassembling chloroplasts. accumulates (Tejos et al., 2010). Overall, embryonic chlo- Available evidence rather suggests that embryonic roplasts resemble mature chloroplasts in leaves, but they photosynthesis could play a role after seed maturation. contain less grana with fewer stacks than leaf chloro- Indeed, previous reports have suggested that embry- plasts, possibly as a result of exposure to far-red enriched onic photosynthesis influences seed germination. In- light within the fruit (Allorent et al., 2015; Liu et al., terestingly, when developing seeds were treated with 2017). As the embryo begins to desiccate, the chloro- DCMU, Allorent et al. (2015) observed that subsequent plasts de-differentiate into nonphotosynthetic plastids, mature seeds exhibited lower longevity and delayed called eoplasts, and the embryo loses its green color, germination. Genetic experiments, using ccb2 mutants, becoming white (Liebers et al., 2017). which are deficient in the assembly of the cytochrome The intriguing biological purpose of embryonic b6f complex that is essential for photosynthesis, further photosynthesis remains poorly understood. Indeed, the confirmed that decreased longevity and delayed ger- developing embryo is surrounded by green, photo- mination resulted from perturbing embryonic rather synthetically active maternal tissues (silique, ovule), than maternal photosynthesis (Allorent et al., 2015). which filter the incoming light toward the embryo and An unavoidable by-product of photosynthesis is 1 render it less suitable for photosynthesis. It has been singlet oxygen species ( O2), which have been impli- suggested, in rapeseed (Brassica napus), maize (Zea cated in retrograde signaling between the plastid and mays), and pea (Pisum sativum), that embryonic photo- the nucleus (Nater et al., 2002; Wagner et al., 2004; Lee synthesis could provide oxygen (O2) and ATP to cells et al., 2007; op den Camp et al., 2013). In a study focused located in the inner parts of the embryo where it was on the plastid proteins EXECUTER1 (EX1) and EX2, shown that the concentration of O2 is limited Kim et al. (2009) provided compelling evidence that 1 (Rolletschek et al., 2003; Borisjuk and Rolletschek, 2009; O2-dependent retrograde signaling during