Molecular evolution of restorer-of-fertility:
the case of sugar beet Rf1

N mito DNA

S mito DNA
Genomerearrangement

S-mito unique protein(preSATP6)

Sugar beet Rf1

Oligomer form

Male sterility
How has sugar beet Rf1 evolved?

Sugar beet Rf1 encodes an Oma1-like protein.
NH2

Mt
signalTM

TMTM

COOH

Supplementary information of Oma1
Oma1 is a ubiquitous gene in eukaryotes. It plays multiple roles
such as;Quality control of mitochondrial inner membrane proteins (yeast).
Inhibiting mitochondrial fusion via OPA1 cleavage (mammal).
KO mutant is viable but exhibits several abnormalities (Arabidopsis).
Oma1 is single copy in most of eukaryotes.

Possible evolutionary relationship between sugar beet Rf1 and Oma1
1. Sugar beet Rf1 is the genuine Oma1.
Arabidopsis

Orthologous

Oma1

Sugar beet
Rf1

2. Sugar beet Rf1 is a derivative of Oma1.
Arabidopsis

Paralogous

Oma1

Sugar beet
Rf1

Orthologous
Oma1

Sugar beet Rf1 is a paralogue of Oma1
Sugar beet genome is examined to find Oma1 homologues.

Sugar beet has several Oma1 copies

Caryophyllales(A)

Amborellales (BM)Poales (M)0.20

In contrast to Arabidopsis, sugar beet has several copies of duplicatedOma1 as lineage specific paralogues.
Arakawa et al. Genome Biology and Evolution, 2020

Evolutionary model of sugar beet Rf1

Arabidopsis

Paralogous

Sugar beet

Oma1

Rf1

Gene
duplication

Orthologous
Oma1

Considering Arabidopsis Oma1 retains ancestral features,
are Arabidopsis Oma1, sugar beet Rf1 and sugar beet Oma1functionally equivalent to each other?

Neither Arabidopsis OMA1 or sugar beet OMA1 binds to preSATP6protein.
35S

atOma1 FLAG35S

bvOma1 FLAG35SRfFLAG

αFLAG
FLAGRfY

preSATP6

OMA1 is inherently unable to bind to preSATP6 protein.
The binding activity may have evolved after the gene duplication.
Arakawa et al. R Soc Open Sci 2019

Meiosis

TetradMicro spore

Arabidopsis Oma1

Sugar beet Oma1

Rf1

Gene expression pattern is different among Arabidopsis Oma1, sugar beet Oma1 and Rf1.

Arakawa et al. R Soc Open Sci 2019

Difference in gene expression pattern between three Oma1-homologues
MeiosisatOma1
bvOma1
Rf1

TetradMicrospore

Tapetum
Meiocyte
Tapetum
MeiocyteTapetum
Meiocyte

1. Rf1 acquired meiosis expression.
2. bvOma1 and Rf1 alternately expresses to complement atOma1
expression pattern.

Evolution of expression pattern after gene duplication is suggested.
Kubo et al. Plants 2020

Evolution of sugar beet Rf1 may be very complex but all have
happened recently.
Ancestral Oma1 may resemble ArabidopsisOma1
Regulatory element

Gene coding region
1. Gene duplication

3. Alteration of regulatory
element
4. Alteration of coding
region2. Alteration ofregulatory element

Sugar beet Oma1

Rf1

Rf1 evolution may be ongoing

Copy number variation (CNV) of Rf1 locus in cultivated beet.
Arakawa et al. BMC Plant Biology, 2020

Rf1 evolution may be ongoing
Genetic action in field
Strong restoration
All copies have potential to bind preSATP6
Weak
Single copy has potential to bind preSATP6

NoNo copy has potential to bind preSATP6
Rf1 is a complex locus whose genetic action is determined by its
constituent copies.
Arakawa et al. BMC Plant Biology, 2020

1. Sugar beet Rf1 is an evolutionarily young gene.
2. Evolution of sugar beet Rf1 is a complex process that includes manysteps such as gene duplication, alterations of coding- andregularory elements, and alteration(s) in the original copy.
3. Sugar beet Rf1 likely continues its evolution to form functionallydifferent alleles (haplotypes).
4.

Evolution of Rf1 locus and resistance (R) gene locus shares somefeatures, such as CNV and positive selection.

References
Arakawa T, et al. How did a duplicated gene copy evolve into a restorer-of-fertility
gene in a plant? The case of Oma1, Royal Society Open Science, 6: 190853, 2019.
Arakawa T, et al. A lineage-specific paralogue of Oma1 evolved into a gene family
from which a suppressor of male sterility-inducing mitochondria emerged in plants.
Genome Biology and Evolution, 12:2314-2327, 2020.
Arakawa T, et al. The molecular basis for allelic differences suggests Restorer-offertility 1 is a complex locus in sugar beet (Beta vulgaris L.). BMC Plant Biology,
20:503, 2020.