Recent Gene Duplication and Subfunctionalization Produced a Mitochondrial GrpE, the Nucleotide Exchange Factor of the Hsp70 Complex, Specialized in Thermotolerance to Chronic Heat Stress in Arabidopsis    

Abstract

The duplication and divergence of heat stress (HS) response genes might help plants adapt to varied HS conditions, but little is known on the topic. Here, we examined the evolution and function of Arabidopsis (Arabidopsis thaliana) mitochondrial GrpE (Mge) proteins. GrpE acts as a nucleotide-exchange factor in the Hsp70/DnaK chaperone machinery. Genomic data show that AtMge1 and AtMge2 arose from a recent whole-genome duplication event. Phylogenetic analysis indicated that duplication and preservation of Mges occurred independently in many plant species, which suggests a common tendency in the evolution of the genes. Intron retention contributed to the divergence of the protein structure of Mge paralogs in higher plants. In both Arabidopsis and tomato (Solanum lycopersicum), Mge1 is induced by ultraviolet B light and Mge2 is induced by heat, which suggests regulatory divergence of the genes. Consistently, AtMge2 but not AtMge1 is under the control of HsfA1, the master regulator of the HS response. Heterologous expression of AtMge2 but not AtMge1 in the temperature-sensitive Escherichia coli grpE mutant restored its growth at 43°C. Arabidopsis T-DNA knockout lines under different HS regimes revealed that Mge2 is specifically required for tolerating prolonged exposure to moderately high temperature, as compared with the need of the heat shock protein 101 and the HS-associated 32-kD protein for short-term extreme heat. Therefore, with duplication and subfunctionalization, one copy of the Arabidopsis Mge genes became specialized in a distinct type of HS. We provide direct evidence supporting the connection between gene duplication and adaptation to environmental stress.

The Significance of Different Diacylgycerol Synthesis Pathways on Plant Oil Composition and Bioengineering

“…The castor PDCT enhanced the accumulation of HFA in TAG of transgenic plants co-expressing the castor FA hydroxylase, consistent with the ability of castor to utilize a PC-derived DAG(2) pathway of TAG synthesis in vivo (Hu et al, 2012). Therefore, the symmetrical activity of PDCT may also be important for channeling de novo DAG(1) substrates into PC for unusual FA synthesis similar to its use in PUFA synthesis in Arabidopsis (Lu et al, 2009).…”

“…An alternative approach could be to redirect the flux of de novo DAG(1) from PC synthesis directly to TAG synthesis. Recent studies co-expressing the castor FA hydroxylase and castor PDCT in Arabidopsis has achieved increased accumulation of HFA in TAG and less in PC, as well as mostly relieving the HFA induced reduced oil phenotype (Hu et al, 2012). However, it is unknown if over-expression of castor PDCT increased the flux of HFA-containing de novo DAG(1) into PC or if the results were due to an increased flux of HFA-containing PC-derived DAG(2) out of PC, thereby reducing HFA acyl editing and synthesis of HFA-containing de novo DAG(1).…”

“…However, it is unknown if over-expression of castor PDCT increased the flux of HFA-containing de novo DAG(1) into PC or if the results were due to an increased flux of HFA-containing PC-derived DAG(2) out of PC, thereby reducing HFA acyl editing and synthesis of HFA-containing de novo DAG(1). Expression of the castor FA hydroxylase in the Arabidopsis pdct mutant reduced HFA accumulation in TAG and total seed oil compared to expression of the FA hydroxylase in wild-type Arabidopsis (Hu et al, 2012). These results support the hypothesis based on the accumulation of HFA at the sn -2 position of TAG (Bates and Browse, 2011; van Erp et al, 2011) that the flux of HFA-containing PC-derived DAG(2) out of PC is important for HFA-TAG accumulation in transgenic Arabidopsis .…”

The Membrane-Bound NAC Transcription Factor ANAC013 Functions in Mitochondrial Retrograde Regulation of the Oxidative Stress Response in Arabidopsis

“…AOX1a function is best studied with respect to mitochondria-initiated oxidative stress responses (Maxwell et al, 1999;Umbach et al, 2005) but is not limited to mitochondrial stress responses as evidenced by its importance in chloroplast protection during high-light stress (Yoshida et al, 2007;Giraud et al, 2008). Furthermore, the MDS is enriched for members of multigene families associated with detoxification pathways (cytochrome P450 monooxygenase, N-acetyltransferase, glycosyltransferase, ATP binding cassette, and multi antimicrobial extrusion protein transporters) (Manabe et al, 2007), together with two mitochondrial proteins (HSP23.5 and MITOCHONDRIAL GroPlike gene E1 [MGE1]) that might have chaperone-like activities (Visioli et al, 1997;Hu et al, 2012). Other Arabidopsis genes that contain evolutionarily conserved MDM instances are also enriched for components of the alternative respiratory chain, proteins involved in multidrug/xenobiotic transport, mitochondrial HSPs, and subunits of the 20S proteasome (see Supplemental Tables 5 and 7 online).…”

Cell Wall Invertase Promotes Fruit Set under Heat Stress by Suppressing ROS-Independent Cell Death

“…The response mechanisms of plants to LMHS may be drastically different from those to SSHS (Yeh et al, 2012;Hancock et al, 2014). For example, mitochondrial cochaperone MGE2 is required for the tolerance of Arabidopsis vegetative growth to LMHS (35°C for 9 d), but not for its response to SSHS (44°C for 150 min; Hu et al, 2012;Yeh et al, 2012). Despite its importance in developing strategies to improve crop adaptability to global warming, information on the effects of LMHS on plant development in general and on early reproductive development in particular remains scarce.…”