An active Mitochondrial Complex II Present in Mature Seeds Contains an Embryo-Specific Iron–Sulfur Subunit Regulated by ABA and bZIP53 and Is Involved in Germination and Seedling Establishment

Abstract

Complex II (succinate dehydrogenase) is an essential mitochondrial enzyme involved in both the tricarboxylic acid cycle and the respiratory chain. In Arabidopsis thaliana, its iron–sulfur subunit (SDH2) is encoded by three genes, one of them (SDH2.3) being specifically expressed during seed maturation in the embryo. Here we show that seed SDH2.3 expression is regulated by abscisic acid (ABA) and we define the promoter region (-114 to +49) possessing all the cis-elements necessary and sufficient for high expression in seeds. This region includes between -114 and -32 three ABRE (ABA-responsive) elements and one RY-enhancer like element, and we demonstrate that these elements, although necessary, are not sufficient for seed expression, our results supporting a role for the region encoding the 5’ untranslated region (+1 to +49). The SDH2.3 promoter is activated in leaf protoplasts by heterodimers between the basic leucine zipper transcription factors bZIP53 (group S1) and bZIP10 (group C) acting through the ABRE elements, and by the B3 domain transcription factor ABA insensitive 3 (ABI3). The in vivo role of bZIP53 is further supported by decreased SDH2.3 expression in a knockdown bzip53 mutant. By using the protein synthesis inhibitor cycloheximide and sdh2 mutants we have been able to conclusively show that complex II is already present in mature embryos before imbibition, and contains mainly SDH2.3 as iron–sulfur subunit. This complex plays a role during seed germination sensu-stricto since we have previously shown that seeds lacking SDH2.3 show retarded germination and now we demonstrate that low concentrations of thenoyltrifluoroacetone, a complex II inhibitor, also delay germination. Furthermore, complex II inhibitors completely block hypocotyl elongation in the dark and seedling establishment in the light, highlighting an essential role of complex II in the acquisition of photosynthetic competence and the transition from heterotrophy to autotrophy.

Genome-Wide Identification and Structural Analysis of bZIP Transcription Factor Genes in Brassica napus

“…The bZIP genes bZIP28 , bZIP2 , bZIP53 , and bZIP60 play positive roles in abiotic stress signaling and responses [ 62 , 63 ], as well as growth and development [ 23 , 64 ]. However, little is known about the roles of BnbZIP13 and BnbZIP41 .…”

Mitochondrial complex II of plants: subunit composition, assembly, and function in respiration and signaling

“…SDH2‐3 is specifically expressed in the embryo during seed development (Elorza et al ., ), and its disruption alone was shown to cause delayed seed germination (Roschzttardtz et al ., ). Recent analysis indicated that SDH2‐3 expression in seed is regulated by ABA, with the promoter region containing three ABA‐responsive elements (Restovic et al ., ). In Solanum lycopersicum (tomato), RNA interference lines of SDH2‐2 showed increased rates of photosynthesis and growth caused by their higher stomatal aperture (Araujo et al ., ), similar to the reported SDH1‐1 / sdh1‐1 plants mentioned above (Fuentes et al ., ).…”

“…Partial inhibition of SDH by the competitive inhibitor malonate or non‐competitive inhibitor TTFA decrease shoot and root growth rate in Arabidopsis (Jardim‐Messeder et al ., ). SDH inhibitors completely block hypocotyl elongation in the dark and seedling establishment in the light, indicating that complex II plays a role in the acquisition of photosynthetic competence and the transition from heterotrophy to autotrophy (Restovic et al ., ). SDH inhibitors are also widely used worldwide as fungicides to prevent the proliferation of molds in cereal crops.…”

Transitioning to the Next Phase: The Role of Sugar Signaling throughout the Plant Life Cycle

“…In developing wheat grains, in vitro SnRK1 activity was reported in the embryo and endosperm, which together with low T6P in the embryo may support high in vivo SnRK1 activity for embryo maturation (Martínez-Barajas et al, 2011). The C/S1 bZIP transcription factors, in particular, bZIP53, which is expressed late during seed development, have also been proposed to be involved in storage protein synthesis and seed maturation Alonso et al, 2009;Restovic et al, 2017).…”