Ameztoy Kinia, Sánchez-López Ángela María, Muñoz Francisco José, Bahaji Abdellatif, Almagro Goizeder, Baroja-Fernández Edurne, Gámez-Arcas Samuel, De Diego Nuria, Doležal Karel, Novák Ondřej, Pěnčík Ales, Alpízar Adán, Rodríguez-Concepción Manuel, Pozueta-Romero Javier
Instituto de Agrobiotecnología (Consejo Superior de Investigaciones Científicas/Gobierno de Navarra), Mutilva, Spain.
Department of Chemical Biology and Genetics, Centre of the Region Haná for Biotechnological and Agricultural Research, Faculty of Science, Palacký University, Olomouc, Czechia.
Front Plant Sci. 2021 Mar 5;12:637976. doi: 10.3389/fpls.2021.637976. eCollection 2021.
Microorganisms produce volatile compounds (VCs) with molecular masses of less than 300 Da that promote plant growth and photosynthesis. Recently, we have shown that small VCs of less than 45 Da other than CO are major determinants of plant responses to fungal volatile emissions. However, the regulatory mechanisms involved in the plants' responses to small microbial VCs remain unclear. In plants exposed to small fungal VCs, growth promotion is accompanied by reduction of the thiol redox of Calvin-Benson cycle (CBC) enzymes and changes in the levels of shikimate and 2-C-methyl-D-erythritol 4-phosphate (MEP) pathway-related compounds. We hypothesized that plants' responses to small microbial VCs involve post-translational modulation of enzymes of the MEP and shikimate pathways via mechanisms involving redox-activated photosynthesis signaling. To test this hypothesis, we compared the responses of wild-type (WT) plants and a mutant defective in a redox-regulated isoform of the CBC enzyme fructose-1,6-bisphosphatase to small VCs emitted by the fungal phytopathogen Fungal VC-promoted growth and photosynthesis, as well as metabolic and proteomic changes, were substantially weaker in plants than in WT plants. In WT plants, but not in plants, small fungal VCs reduced the levels of both transcripts and proteins of the stromal Clp protease system and enhanced those of plastidial chaperonins and co-chaperonins. Consistently, small fungal VCs promoted the accumulation of putative Clp protease clients including MEP and shikimate pathway enzymes. and mutants with disrupted plastidial protein homeostasis responded weakly to small fungal VCs, strongly indicating that plant responses to microbial volatile emissions require a finely regulated plastidial protein quality control system. Our findings provide strong evidence that plant responses to fungal VCs involve chloroplast-to-nucleus retrograde signaling of redox-activated photosynthesis leading to proteostatic regulation of the MEP and shikimate pathways.
微生物会产生分子量小于300道尔顿的挥发性化合物（VCs），这些化合物可促进植物生长和光合作用。最近，我们发现除一氧化碳外，分子量小于45道尔顿的小VCs是植物对真菌挥发性物质排放作出反应的主要决定因素。然而，植物对小微生物VCs作出反应所涉及的调控机制仍不清楚。在暴露于小真菌VCs的植物中，生长促进伴随着卡尔文-本森循环（CBC）酶的硫醇氧化还原作用降低以及莽草酸和2-C-甲基-D-赤藓糖醇4-磷酸（MEP）途径相关化合物水平的变化。我们推测，植物对小微生物VCs的反应涉及通过氧化还原激活的光合作用信号传导机制对MEP和莽草酸途径的酶进行翻译后调控。为了验证这一假设，我们比较了野生型（WT）植物和一种在CBC酶果糖-1,6-二磷酸酶的氧化还原调节同工型中存在缺陷的突变体对真菌植物病原体释放的小VCs的反应。真菌VCs促进的生长和光合作用以及代谢和蛋白质组学变化在突变体植物中比在WT植物中要弱得多。在WT植物中，而非突变体植物中，小真菌VCs降低了基质Clp蛋白酶系统的转录本和蛋白质水平，并提高了质体伴侣蛋白和共伴侣蛋白的水平。一致的是，小真菌VCs促进了包括MEP和莽草酸途径酶在内的假定Clp蛋白酶底物的积累。质体蛋白质稳态被破坏的突变体对小真菌VCs反应微弱，这有力地表明植物对微生物挥发性物质排放的反应需要一个精细调节的质体蛋白质质量控制系统。我们的研究结果提供了强有力的证据，表明植物对真菌VCs的反应涉及氧化还原激活的光合作用的叶绿体到细胞核逆行信号传导，从而导致对MEP和莽草酸途径的蛋白质稳态调节。
