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BABY BOOM (BBM): a candidate transcription factor gene in plant

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DOI: 10.1007/s10529-018-2613-5

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BABY BOOM (BBM): a candidate
transcription factor gene in plant
biotechnology

Priyanka Jha & Vijay Kumar

Biotechnology Letters

ISSN 0141-5492
Volume 40
Combined 11-12

Biotechnol Lett (2018) 40:1467-1475

DOI 10.1007/s10529-018-2613-5

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REVIEW

BABY BOOM (BBM): a candidate transcription factor gene

in plant biotechnology
Priyanka Jha . Vijay Kumar

Received: 25 June 2018 / Accepted: 4 October 2018 / Published online: 8 October 2018
Ó Springer Nature B.V. 2018

Abstract Plants have evolved a number of tran- Keywords BABY BOOM (BBM)
Cell
scription factors, many of which are implicated in proliferation
Embryogenesis
Transformation
signaling pathways as well as regulating diverse
cellular functions. BABY BOOM (BBM), transcription
Abbreviations
factors of the AP2/ERF family are key regulators of
ABI3 Abscisic acid insensitive 3
plant cell totipotency. Ectopic expression of the BBM
AP2 APETALA2 DNA-binding domain in plant
gene, originally identified in Brassica napus, has
proteins
diverse functions in plant cell proliferation, growth
BBM BABY BOOM
and development without exogenous growth regula-
CHX Cycloheximide
tors. The BBM gene has been implicated to play an
CRE Creates recombination
important role as a gene marker in multiple signaling
DEX Dexamethasone
developmental pathways in plant development. This
ERF Ethylene-responsive element binding factor
review focuses on recent advances in our understand-
FUS3 FUSCA3
ing of a member of the AP2 family of transcription
GR Glucocorticoid receptor
factor BBM in plant biotechnology including plant
GUS b-Glucuronidase
embryogenesis, cell proliferation, regeneration, plant
LEC LEAFY COTYLEDON
transformation and apogamy. Recent discoveries
ORF Open reading frame
about the BBM gene will inevitably help to unlock
PKL PICKLE
the long-standing mysteries of different biological
PRC Polycomb repressive complex
mechanisms of plant cells.
RACE Rapid amplification of cDNA ends
RT- Real-time-polymerase chain reaction
PCR
P. Jha
Amity Institute of Biotechnology (AIB), Amity SE Somatic embryogenesis
University, Kolkata Campus, Kolkata, TAA1 Tryptophan aminotransferase of
West Bengal 700156, India Arabidopsis 1
WUS WUSCHEL
V. Kumar (&)
School of Life Sciences, Research Centre for Plant
Growth and Development, University of KwaZulu-Natal,
Pietermaritzburg, Private Bag X01, Scottsville 3209,
South Africa
e-mail: [email protected]

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Introduction formation, somatic embryogenesis (SE) induction,

development, promoting apogamy and stimulating
The ability to regenerate new tissue, organs (pluripo- transformation (Boutilier et al. 2002; Passarinho et al.
tency) or embryos (totipotency) via tissue culture is a 2008; Heidmann et al. 2011; Lowe et al. 2016;
much-applied phenomenon in plant biotechnology. Horstman et al. 2017a; Bui et al. 2017) (Fig. 1).
In vitro plant regeneration is an important model However, the molecular mechanism which regulates
system in modern crop breeding and has remarkable these biological functions is not clear. As shown in
potential for biotechnological application. The genetic Fig. 1, several regulatory genes such as PICKLE
basis for changes in in vitro regeneration potential still (PKL) and Polycomb repressive complex1/2 (PRC1/2)
remains unclear. However, studies on the genetic subsequently induce the BBM transcription factor
mechanisms that control in vitro regeneration suggest gene. The BBM gene transcriptionally regulates
that a number of transcription factor genes which have LEAFY COTYLEDON1 (LEC1), LEAFY COTYLE-
been identified, are specifically activated or differen- DON2 (LEC2) and AGAMOUS-LIKE15 (AGL15)
tially expressed during plant embryogenesis when genes during SE to promote embryonic competence.
somatic cells are converted into embryonic cells LEC1 expressed the YUC gene, which encodes a
(Chugh and Khurana 2002; Boutilier et al. 2002; biosynthesis enzyme, whereas LEC2 and AGL15
Rojas-Herrera et al. 2002; Schrader et al. 1997; Hu induces the IAA30 (negative regulator of auxin
et al. 2005; Rupps et al. 2016; Zhai et al. 2016). signaling) (Braybrook et al. 2006; Zheng et al. 2009;
Among the genes involved in plant embryogenesis, the Kumar and Van Staden 2017). In addition, the BBM
BABY BOOM (BBM) gene has an important role gene binds to TAA1 and YUC gene, which encodes an
(Boutilier et al. 2002). The BBM gene, which is auxin biosynthesis enzyme (Horstman et al. 2017a).
preferentially expressed, activates a signal transduc- To the best of our knowledge, there is no review
tion pathways leading to the induction of differenti- available on BBM transcription factor gene. The main
ated somatic cells and somatic embryo formation objective of this review is to present a brief update on
(Boutilier et al. 2002). The BBM gene encodes the the current status and recent advances in understand-
APETALA2 (AP2) FAMILY/ETHYLENE- ing the diverse functions of the BBM gene and provide
RESPONSIVE ELEMENT BINDING FACTOR insights into the discovered BBM gene functions in
(AP2/ERF) domain transcription factor, which has plant embryogenesis, growth and development.
diverse functions in cell proliferation, plant growth
and development (Riechmann and Meyerowitz 1998;
Nole-Wilson et al. 2005; Feng et al. 2005; Floyd and BBM transcription factor is a key marker gene
Bowman 2007; Passarinho et al. 2008; Ouakfaoui in plant embryogenesis
et al. 2010) (Table 1). The BBM gene was first isolated
as a marker from embryogenic cells in microspore- The developmental pathway of SE involves complex
derived tissue culture and was shown to induce cellular reprogramming and activation of various
somatic embryos when ectopically expressed in signaling pathways. A number of molecular genetics
Brassica napus (Boutilier et al. 2002). The BBM gene studies suggest that ectopic expression of transcription
induces embryogenesis in differentiated cells under factor genes induce spontaneous SE (Salvo et al. 2014;
culture conditions that normally do not support in Horstman et al. 2017a, b). The BBM transcription
wild-type plants and possibly acts as a key regulator of factor gene is a key regulator of plant cell totipotency,
plant embryonic development (Boutilier et al. 2002). which is ectopically expressed and induces SE without
The role of the BBM gene has been linked to plant exogenous plant growth regulators or stress (Boutilier
embryogenesis in many plant species such as Ara- et al. 2002; Horstman et al. 2017a). Ectopic expression
bidopsis thaliana (Boutilier et al. 2002), Brassica of the BBM gene stimulated signaling pathways that
napus (Boutilier et al. 2002), Glycine max L. (Ouak- promoted cell division and dedifferentiation. How-
faoui et al. 2010), Capsicum annuum L. (Irikova et al. ever, this process was not dependent on the addition of
2012) and Zea mays (Salvo et al. 2014). The BBM gene auxin/cytokinin but could be improved with the
acts as a possible biomarker and is involved in multi- addition of these plant growth regulators (Boutilier
tasking functions including cell proliferation, shoot et al. 2002).

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Table 1 Showing BBM and BBM-like reported gene from different plant species and their biological functions in plant growth and
development
Plant species Eudicot/monocot Gene Name of gene Biological function References
type

Brassica Eudicot BBM BnBBM Cell proliferation, morphogenesis during Boutilier et al.
napus embryogenesis (2002)
Arabidopsis Eudicot BBM AtBBM Cell proliferation, spontaneous formation of Boutilier et al.
thaliana somatic embryos, cotyledon-like structures on (2002)
seedlings
Arabidopsis Eudicot BBM BBM:GR Activates a complex developmental pathways Passarinho
thaliana into cell proliferation and cell growth et al. (2008)
Arabidopsis Eudicot BBM BBM Cell proliferation and somatic embryogenesis Kulinska-
thaliana Lukaszek
et al. (2012)
Arabidopsis Eudicot BBM BBM:GR Improve plant regeneration and yield fertile Lutz et al. 2015
thaliana plants
Nicotiana Eudicot BBM AtBBM; BnBBM Cell proliferation and differentiation Srinivasan
tabacum L. (heterologous et al. (2007)
gene)
Glycine max Eudicot BBM GmBBM Somatic embryogenesis and embryo Ouakfaoui
L. development et al. (2010)
Rosa canina Eudicot BBM RcBBM1 Improve shoot regeneration efficiency Yang et al.
RcBBM2 (2014)
Theobroma Eudicot BBM TcBBM Enhance somatic embryogenesis without Florez et al.
cacao compromising plant growth and development (2015)
Capsicum Eudicot BBM BnBBM Used to efficiently regenerate transgenic plants Heidmann
annuum through Agrobacterium-mediated et al. (2011)
transformation
Coffeaarabica Eudicot BBM CaBBM In vitro embryogenic process Silva et al.
(2015)
Sorghum Monocot BBM Maize BBM Improve transformation efficiency Lowe et al.
bicolor (2016)
Saccharum Monocot BBM Maize BBM Improve transformation efficiency Lowe et al.
officinarum (2016)
Oryza sativa Monocot BBM Maize BBM Improve transformation efficiency Lowe et al.
(2016)
Sorghum Monocot BBM Maize BBM Effiecient Agrobacterim-mediated Mookan et al.
bicolor transformation (2017)
Musa Monocot BBM MaBBM1 Induction of somatic embryogenesis Shivani et al.
acuminata MaBBM2 (2017)
Pennisetum Monocot BBM PsASGR-BBML Induction of apomixis Conner et al.
glaucum (2015)
Ceratopteris Fern BBM BnBBM Promote apogamy Bui et al.
richardii (2017)

In Brassica napus, two BBM genes (BnBBM1 and 2002). Brassica and Arabidopsis plants transformed
BnBBM2) and in Arabidopsis thaliana a single with UBI::BBM and 35S::BBM constructs respec-
ortholog (AtBBM) were identified. Overexpression of tively produced cotyledon-like somatic embryos on
these genes revealed enhanced cell proliferation and post germination organs. In addition, ectopic BBM
morphogenesis during embryogenesis (Boutilier et al. expression induced a variety of different pleiotropic

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Fig. 1 Schematic overview of the BABY BOOM (BBM) transcription factor gene that may regulate diverse functions of plant growth
and development

phenotypes such as pinched or lobed cotyledons, GmAIL5 and GmPLT2 were similar to Arabidopsis
thickened or callused hypocotyls, short shoots, for- AINTEGUMENTA-like (AIL5) and PLETHORA2
mation of ectopic shoots, callus formation and antho- (PLT2) respectively. Sequence comparison of BBM
cyanin accumulation on vegetative and regenerative orthologues identified the presence of five motifs in
development at a low penetrance in UBI::BBM and the N-terminal, and five motifs in the C-terminal
35S::BBM Brassica and Arabidopsis transgenic seed- sequences. In the N-terminal sequences, the fourth
lings respectively. However, these phenotypes were motif (bbm-1) was specific to BBM-like genes,
variable within and between Brassica and Arabidopsis whereas in the C-terminal sequences, all five motifs
transgenic lines (Boutilier et al. 2002). These results were conserved with a low level of specificity. The
suggest that the BBM gene regulates signaling path- function of the bbm-1 sequence motif in SE and
ways for SE and act as a plant hormone stimulator. embryo development regulation was further detected
Overexpression of BBM-mediated SE enhanced by deletion and domain swap analysis. Further exam-
plant regeneration in Populus tomentosa (Deng et al. ination indicated that, bbm-1 was linked to the one
2009). Ectopic expression of BBM induced somatic other euANT2 motif, which was identified in the
embryos formation from Chinese white poplar callus. euANT lineage including PLT2 and AIL5 genes. A
A total of 12 somatic embryos were induced from 6 deletion of the euANT2 motif singly and together with
calli after 4 weeks of culture. Out of these 12, only 6 bbm-1 prevented somatic embryos from generating
somatic embryos were germinated and converted into shoots after prolonged times in culture (Ouakfaoui
plantlets (Deng et al. 2009). et al. 2010). These results provide an understanding of
The BBM gene is also involved in SE and embryo the mechanism by which BBM governs
development in Glycine max L. (soyabean) (Ouak- embryogenesis.
faoui et al. 2010). Three AP2 gene families, GmBBM1, In Theobroma cacao, a BBM gene (TcBBM) was
GmAIL5 and GmPLT2 were identified and isolated cloned and expressed to promote the transition of
from embryonic cultures of Glycine max L. (soybean). somatic T. cacao cells from vegetative to embryonic
The GmBBM1 sequence showed high similarity growth (Florez et al. 2015). The TcBBM expression
([ 91%) to AtBBM and BnBBM genes, whereas level was observed throughout the embryo

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development; globular, heart, early torpedo, late and growth (Passarinho et al. 2008). By using DNA
torpedo and mature somatic embryo stages. Overex- microarray analysis in combination with post-transla-
pression of TcBBM in T. cacao led to phenotype, tionally regulated BBM:GR protein and cyclohex-
which did not require exogenous hormones for direct imide (CHX), a number of target genes have been
embryogenesis. However, transient expression of identified which are directly activated by BBM gene
TcBBM improved embryogenic potential. These expression. A number of target genes encoding
results indicated that TcBBM has an important role proteins have been shown to be expressed and
in SE and its transcription level could serve as a involved in cellular signaling and cell wall modifica-
biomarker for embryonic growth in T. cacao tissue tions (Passarinho et al. 2008).
(Florez et al. 2015). Srinivasan et al. (2007) examined the ectopic
In a recent report, Horstman et al. (2017a) demon- expression of BBM on tobacco (Nicotiana tabacum)
strated that the BBM gene works as a major regulator development and regeneration capacity. Eight trans-
for plant cell totipotency. BBM transcriptionally genic tobacco lines expressed the 35S::AtBBM con-
regulated LEC1/2, FUSCA3 (FUS3) and ABSCISIC struct and twenty transgenic tobacco lines expressing
ACID INSENSITIVE (ABI3) gene networks. These the 35S::BnBBM construct. They exhibited a number
results also suggested that LEC2 and ABI3 are positive of similar phenotypes including leaf rumpling, callus
regulators of BBM-mediated embryogenesis, where as formation and sterility. However, no adventitious
LEC1 and FUS3 are essential for SE. BBM-induced SE shoot formation and somatic embryo formation was
is a dose and context-dependent mechanism. High observed on the 35S::BBM tobacco lines (Srinivasan
BBM doses induce SE, whereas lower doses induce et al. 2007).
organogenesis. However, no cell differentiation was Two BBM orthologue genes RcBBM1 and RcBBM2
found in the lowest BBM dose. This study also were isolated by a combination of degenerate PCR and
hypothesized that BBM-mediated embryogenesis was RACE from Rosa canina (Yang et al. 2014). The
enhanced by LAFL gene expression (Horstman et al. sequence analysis revealed that the RcBBM1 (2936 bp
2017a). The BBM gene has emerged as important in length) encodes a predicted protein of 832 amino
transcription factor that control embryogenesis and acids and comprises an ORF of 2499 bp, whereas
has considerable potential in plant biotechnology. RcBBM2 (2921 bp in length) contained an ORF of
These results suggest that the BBM gene acts as a key 2487 bp and encodes a predicted protein of 828 amino
regulator for plant cell totipotency and plant embryo acids. Both genes showed as candidate markers for
identity. In addition, it provides new insight into the improving shoot regeneration capacity in R. canina.
molecular mechanism by which the BBM gene con- By using confocal microscopic examination, it was
trols SE. However, the exact mechanism of the BBM revealed that RcBBM1 and RcBBM2 were both
gene controlling signaling transmission specificity to nucleus-localized proteins. The overexpression of
regulate somatic embryo formation remains unclear. RcBBM1 and RcBBM2 transgenic line in A. thaliana
was characterized in shoot regeneration and SE using
RT-PCR (Yang et al. 2014). The results suggested that
BBM transcription factor enhances cell RcBBM1 and RcBBM2 are candidate genes for
proliferation and regeneration promoting shoot regeneration capacity in R. canina,
allowing further research on RcBBMs in spontaneous
Overexpression of native and heterologous BBM production of somatic embryos.
genes are also responsible for the induction of cell Lutz et al. (2015) described novel improved plant
proliferation and regeneration in different plant regeneration in A. thaliana through a steroid-inducible
species (Srinivasan et al. 2007; Morcillo et al. 2007; BBM system that resulted in fertile and diploid plants.
Passarinho et al. 2008; Bandupriya et al. 2014; Yang Two steroid-inducible BBM constructs BBM:GR and
et al. 2014; Lutz et al. 2015) It has also been used to BBM:GFP:GR were created. The BBM coding region
promote apogamy in ferns (Bui et al. 2017). fused with the glucocorticoid receptor (GR) steroid-
The BBM gene is expressed as a marker and binding domain and BBM:GFP:GR fusion facilitated
activates a complex signaling network of different the visualization of BBM movement. In the absence of
developmental pathways linked to cell proliferation synthetic steroid dexamethasone (DEX), the BBM:GR

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fusion protein was localized in the cytoplasm. How- no transgenic plantlets were obtained from any pepper
ever, in the presence of DEX in the culture medium, variety. Average transformation efficiency 0.6 and
BBM transcription factor translocated from the cyto- 1.1% were obtained for Fiesta and Ferrari pepper
plasm to the nucleus, hence activating genes involved varieties, respectively (Heidmann et al. 2011).
in embryogenesis. In the presence of DEX, the leaf Overexpression of the BBM gene was used to
section produced shoots and callus whereas, removal produce transgenic Populus tomentosa (Chinese white
of DEX allowed seed formation and flowering. poplar) (Deng et al. 2009). BBM overexpression
However, few shoot regeneration was observed in developed somatic embryos from Chinese white
the absence of DEX using flow cytometry. Increased poplar calli, which were converted into plantlets.
ploidy levels were also noted in the regenerated plants However, no regeneration was obtained from untrans-
(Lutz et al. 2015). Together, these results indicated formed calli. To produce marker-free lines, the system
that the BBM gene plays an essential role in cell was combined with heat shock-inducible FRT/FLP
proliferation and regeneration. The BBM gene regu- (site-specific recombination system from Saccha-
lated a complex network of developmental pathways romyces cerevisiae) system (Deng et al. 2009). This
associated with cell proliferation and regeneration. In study also confirmed that the BBM gene acts as a
addition, the BBM gene was found as a candidate positive selectable marker for Chinese white poplar
marker for improving shoot regeneration efficiency. transformation, and transgenic poplar plants can be
obtain without the use of any antibiotic or herbicide
resistance genes (Deng et al. 2009).
BBM transcription factor gene is crucial in plant In a promising breakthrough report by Lowe et al.
transformation (2016) the BBM gene was shown to improve monocot
transformation in several commercial genotypes.
Plant transformation is commonly mediated by Overexpression of Zea mays (maize) BBM gene and
Agrobacterium, where protoplast and particle bom- WUSCHEL2 (WUS2) stimulated transformation fre-
bardment has enabled novel insights into plant biol- quency in Saccharum officinarum (sugarcane) callus,
ogy. Standard plant transformation is hampered by Oryza sativa ssp. Indica (rice) callus and Sorghum
long turnaround times to recover transgenic plants as bicolor (sorghum) immature embryos. The BBM gene
well as several technical bottlenecks (Altpeter et al. transformed directly into leaf segment from seedlings
2016; Mookan et al. 2017). Recent research reports or embryo from mature seeds in a variety of pioneer
offer a promising breakthrough solution to many inbred lines (PHH5G). The recovery of one inbred
obstacles where plant transformation is improved maize line without the use of a selectable marker was
using morphogenic regulators to mediate transforma- also reported. These results indicated a dramatic
tion (Heidmann et al. 2011; Lowe et al. 2016; increase in transformation frequencies through over-
Svitashev et al. 2016; Mookan et al. 2017). expression of BBM and WUS2 and a strong depen-
The overexpression of the BBM gene has been used dence on the promoters used to drive the BBM and
as a biotechnology tool to improve transformation in WUS2 morphogenic regulators (Lowe et al. 2016).
model and crop species (Deng et al. 2009; Heidmann More recently, by using co-expression of maize
al. 2011; Lutz et al. 2011; Florez et al. 2015; Lowe BBM and WUS2 transcription factor genes, an efficient
et al. 2016). The ectopic expression of B. napus BBM Agrobacterium-mediated transformation was identi-
(BnBBM) transcription factor was used to efficiently fied in sorghum without the use of a chemical
regenerate transgenic plants from Capsicum annuum selectable marker (Mookan et al. 2017). In addition,
(Sweet pepper) varieties (Heidmann et al. 2011). The a reliable and increased transformation frequency was
C. annuum explants were co-cultivated with the established for of the recalcitrant B73 (maize inbred)
35S:BnBBM:GR construct carrying the GUS and sorghum (P898012 genotypes) varieties via co-
selectable marker and this improved transformation expression of BBM and WUS. The PHP78891 vector
efficiency for each of the pepper (Fiesta, Ferrari and comprised CRE:WUS2:BBM cassette, bracketed by
Spirit) varieties. Out of three pepper varieties, trans- lox P sites. Transgenic introduction of this expression
genic plantlets were produced for only two varieties vector showed transient expression of GFP in early
(Fiesta and Ferrari). However in control experiments, and late somatic embryos, shoots, vegetative organs

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and pollen. By using molecular analysis (PCR and and excess in shoot regeneration. CrANT, (a fern
southern blotting), regenerated maize B73 and sor- homolog of the Arabidopsis ANT gene), knockdown
ghum P898012 plants were confirmed to be trans- reduced the gametophyte response to sugar-induced
genic. A significantly increased transformation apogamy (Bui et al. 2017). These results indicated that
frequency for B73 (15%) and P898012 genotypes BnBBM promote cell differentiation and trigger
(6.2%) were noted without the use of a developmental pathways in C. richardii. In future,
selectable marker (Mookan et al. 2017). These results more comprehensive analysis may provide new
indicated that technology for plant transformation is insights to decipher the puzzle of molecular mecha-
entering a new era and these results can extend the use nism underlying in apogamy.
of transient expression of morphogenic regulators
without a selectable marker to overcome transforma-
tion barriers. In future, the role of BBM gene would Conclusions and future perspectives
increase the knowledge in unknown signaling path-
ways stimulating transformation. BBM transcription factor has emerged as an important
gene marker that controls diverse aspects of plant
growth and development and has considerable poten-
BBM-mediated apogamy tial for plant biotechnological application. Many
research reports on the precise expression of the
In plants, naturally occurring mode of asexual repro- BBM gene provides novel evidence on its role in plant
duction through non-zygotic embryogenesis is known embryogenesis. We also note that there is clear
as apogamy. This allows reproduction via seeds evidence that the BBM gene exerts distinct functions
without meiosis and fertilization (Nogler 1984; in different physiological and developmental signal-
Tucker et al. 2003; Bui et al. 2017). ing pathways. In this review, we emphasized diverse
In Pennisetum glaucum (pearl millet), PsASGR- functions of plant cell proliferation, growth and
BABY BOOM-LIKE (PsASGR-BBML) is expressed as development regulated by BBM gene. The BBM gene
a marker gene for apomixis (Conner et al. 2015). By acts as a candidate gene marker to participate in
using RT-PCR, it was demonstrated that the PsASGR- diverse developmental responses and signaling path-
BBML gene is expressed in egg cells, which induce ways, but it is still unclear how the BBM-mediated
parthenogenesis before fertilization and also produce signaling pathways determine specificity. In addition,
the haploid offspring in transgenic pearl millet (Con- how the BBM gene controls signaling transmission
ner et al. 2015). This study also suggested that specificity to regulate somatic embryo formation, cell
PsASGR-BBML plays a significant role as a transcrip- differentiation, plant growth and transformation
tion factor to promote parthenogenesis and embryo remains unclear.
development without fertilization. Future research will be required on the efficient
In a recent promising report, ectopic expression of transformation system to better understand BBM gene
the BBM gene was shown to promote apogamy in a function. This should further reveal the individual
non-vascular plant Ceratopteris richardii (Bui et al. target gene functions to determine the transformation
2017). Ectopic expression of B. napus BBM (BnBBM) efficiency, somatic embryo induction, plant growth
transgene in C. richardii promoted spontaneous pro- and development. Further investigations of the BBM
duction of apogamy without sugar supplement. In C. gene would increase knowledge in unknown signaling
richardii, the BnBBM gene was ectopically expressed pathways, will open new avenues into the activation
using an Agrobacterium-mediated transformation and mechanisms and provide new insights on the signaling
spontaneous apogamy was observed in transgenic specificity. It would also help in a better understanding
gametophytes. Overexpression of BnBBM showed of the complex interaction of gene regulation and other
various phenotypic effects on gametophyte genera- roles of the BBM gene in plant cells.
tions such as increased transformation efficiency,
cordate shape deviation of gametophytes and callus Acknowledgements We apologize to all those colleagues
whose outstanding contributions we could not cite in this
induction. In the sporophyte generation, BnBBM
review. We thank Dr. Wendy Stirk (University of KwaZulu-
expression resulted in adventitious shoot development

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Natal, South Africa) for thorough language correction and the BABY BOOM transcription factor. Plant Cell Rep
reading the manuscript. We also thank the anonymous reviewers 30:1107–1115
for their suggestions, which helped to improve the manuscript. Horstman A, Li M, Heidmann I, Weemen M, Chen B, Muino
JM, Angenent GC, Boutilier K (2017a) The BABY BOOM
Compliance with ethical standards transcription factor activates the LEC1-ABI3-FUS3-LEC2
network to induce somatic embryogenesis. Plant Physiol
Conflict of interest The authors declare that they have no 175:848–857
conflict of interest. Horstman A, Bemer M, Boutilier K (2017b) A transcriptional
view on somatic embryogenesis. Regeneration 4:201–216
Hu H, Xiong L, Yang Y (2005) Rice SERK1 gene positively
regulates somatic embryogenesis of cultured cells and host
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