Decoding the dual function of NAD-malic enzyme: from a universal role in malate respiration to a specific function in C4 photosynthesis
Final Report Abstract
In summary, we found that a duplication of the NAD-ME gene during the evolution of vascular plants resulted in two paralogs lineages, α- and β-NAD-ME, which were retained during seed plant evolution and diversification. We propose that the heteromeric assembly of NAD-ME was established by subfunctionalization of the duplicated NAD-ME genes. Later, neofunctionalization optimized the α- and β-NAD-ME functions and changes in the subunitspecific duplications provided the basis for the recruitment of NAD-ME in C4 biochemistry. We found that in Cleomaceae all NAD-ME genes were affected by C4 evolution, where one of the β-NAD-ME gene copies was co-opted for its function in the C4 pathway. We found that in bundle sheath cell mitochondria of C4 species, the functions of NAD-ME as C4 photosynthetic decarboxylase and as a housekeeping enzyme coexist and are performed by isoforms that combine the same α subunit with differentially adapted β subunits. We described how the neofunctionalization of a heteromeric enzyme can occur through the duplication and subsequent adaptation of one subunit, while the other subunit is shared between the original and new enzyme. Our work paves the way to elucidating the molecular mechanism underlying protein recruitment for novel functions, especially for proteins with heteromeric composition. Specifically, our work shows that a C4-exclusive NAD-ME isoform exists in plant cell mitochondria, which is formed through the differential assembly of protein subunits that accumulated adaptive mutations during evolution. This discovery will now aid in introducing C4 traits into C3 plants. Ongoing projects can now rationally design the incorporation of a NAD-ME with C4 characteristics by introducing the NAD-MEβ1 of C4 Cleome or modifying a preexisting extra NADMEβ copy.
Publications
- (2018) Biochemical control systems for small molecule damage in plants. Plant Signal. Behav. 13, e1477906
Hüdig M, Schmitz J, Engqvist MKM, and Maurino VG
(See online at https://doi.org/10.1080/15592324.2018.1477906) - (2020) Independent recruitment of duplicated β-subunit-coding NAD-ME genes aided the evolution of C4 photosynthesis in Cleomaceae. Front. Plant Sci.
Tronconi MA, Hüdig M, Schranz ME, and Maurino VG
(See online at https://doi.org/10.3389/fpls.2020.572080) - (2020) Single organelle function and organization as estimated from Arabidopsis mitochondrial proteomics. Plant J. 101, 420-441
Fuchs P, Rugen N, Carrie C, Elsässer M, Finkemeier I, Giese J, Hildebrandt TM, Kühn K, Maurino VG, Ruberti C, Schallenberg-Rüdinger M, Steinbeck J, Braun H-P, Eubel H, Meyer E, Müller-Schüssele SJ, and Schwarzländer M
(See online at https://doi.org/10.1111/tpj.14534) - (2021) Respiratory and C4-photosynthetic NAD-malic enzyme coexist in bundle sheath cells mitochondria and evolved via association of differentially adapted subunits
Hüdig M, Tronconi MA, Zubimendi JP, Sage TL, Poschmann G, Bickel D, Gohlke H, and Maurino VG
(See online at https://doi.org/10.1101/2021.06.16.448762) - (2021) Respiratory and C4-photosynthetic NAD-malic enzyme coexist in bundle sheath cells mitochondria and evolved via association of differentially adapted subunits. The Plant Cell
Hüdig M, Tronconi MA, Zubimendi JP, Sage TL, Poschmann G, Bickel D, Gohlke H, and Maurino VG
(See online at https://doi.org/10.1093/plcell/koab265)
