1. INTRODUCTION
Wheat
production plays an important role in global food security, but it is
limited to only one or two generations per year due to time-consuming
field growth (Mueller et al. ,
2012).
To accelerate the developmental rate of plants, controlled environment
agriculture independent of outdoor conditions has been proposed, which
allows for multiple harvests throughout the year (van Delden et
al. ,
2021).
Wheat is typically a long-day plant, and a long photoperiod can promote
early flowering of wheat up to six generations per year in a controlled
environment (Watson et al. , 2018), which is predicted to be a
promising option for increasing future crop production (Asseng et
al. , 2020). Grains per spike is one of the most important
contributors to yield in wheat, but early flowering induced by a long
photoperiod usually sacrifices grains (Ghiglione et al. , 2008;
Rossi et al. , 2015). The contradiction between ”early flowering”
and ”high yielding” is widespread, hampering further improvement of the
annual wheat yield. Outside of the photoperiod, light spectral quality
is also an important light variable that has a profound effect on plant
growth and development (Lazzarin et al. , 2021). For example, red
light has outstanding potential for increasing wheat grains (Dreccer et
al. , 2022). Is it possible to attain “early flowering” and
“high yielding” simultaneously in
wheat cultivation using the long photoperiod supplemented with red light
regimen?
Grains per spike in wheat is composed of spikelets per spike coupled
with grains per spikelet (Gauley & Boden, 2019). Studies have found
that adding more spikelets, like paired spikelets (Boden et al. ,
2015) and supernumerary spikelets (Li K et al. , 2021; Wang et
al. , 2022), can make more wheat grains. When spikelets remain
constant, it is necessary to look into ways to increase grains even
more. As a cleistogamous species, the number of wheat grains at maturity
is largely determined by the number of fertile florets per spike (NFFs)
at flowering (Figure S1a; Ferrante et al. , 2020). In general, up
to 6-12 floret primordia are produced in a spikelet; however, only a
small proportion of them develop into fertile florets, while others
degenerate (Prieto et al. , 2018).
Floret
primordia are initiated and developed asynchronously in a spike and thus
have uncertain fates (fertility or infertility at flowering), presenting
a great opportunity to increase NFFs and grains by manipulating floret
primordia development. Since stems and spikes are both growing rapidly
during floret development, there is intensive intra-plant competition
for available
assimilates.
In studies with prolonged photoperiod conditions or
photoperiod-insensitive genes, NFFs and grains went down due to
decreased assimilate accumulation in the spike (Ghiglione et al. ,
2008; Prieto et al. , 2018); in contrast, sucrose-feeding
(Ghiglione et al. , 2008) and well-watered conditions (Zhang et
al. , 2020) suggested that increasing assimilate accumulation in
the spike could increase floret survival rate and NFFs. Other studies,
however, found that although low red/far red ratios reduced competition
for assimilates in the uppermost stem (Casal, 1993) or improved
assimilate availability in the spike delayed the death of abortive
floret primordia (Zhang et al. , 2021), they did not increase
NFFs. Focusing on the number of floret primordia and ignoring the
morphological differences demonstrated by floret primordia may result in
a different effect of assimilate availability on floret development and
NFFs. Floret primordia that develop into or beyond the green anther and
elongated stigma branch state (i.e., W7.5 according to the Waddington
scale; Waddington et al. , 1983) usually become fertile florets at
flowering (Zhang et al. , 2021). Similarly, we found that floret
primordia with morphological scores greater than W7.5 at the onset of
some floret primordia degeneration had a reliable potential to achieve
fertility at flowering (R2 = 0.89, Figure S1b) and
were therefore referred to as fertile floret primordia (Figure S1c).
The
development of all floret primordia in a wheat spike is a complex
process that lasts about 30 days from the terminal spikelet stage to
flowering stage. However, the variation in primordia quantity and
morphology during this process, as well as their relationship to
assimilate availability, is not well understood.
Flowering
time is an important selection characteristic for crop improvement.
Numerous genes involved in light-induced flowering have been identified.
For
example, overexpression of the circadian clock gene GIGANTEA (GI)can accelerate wheat flowering (Zhao et al. , 2005); the zinc
finger transcription factor gene CONSTANS (CO ), which is
controlled by GI , induces flowering when CO expression
coincides with light (Valverde et al. , 2004); and the floral
integrator gene FLOWERING LOCUS T (FT ) is activated by
high CO expression in long-day plants (Nicolas Freytes et
al. , 2021). Meanwhile, grains per spike is also a crucial
selection feature for crop improvement and is influenced by the fate of
each floret primordium. Many regulators responsible for floret fertility
have been identified. For instance,
defective
expression of UNDEVELOPED TAPETUM1 (UDT1 ) andPERSISTENT TAPETAL CELL1 (PTC1 ) results in abnormal anther
and pollen morphology, leading to male infertility (Li et al. ,
2011; Yang et al. , 2019); aldehyde dehydrogenase (ALDH) activity
provided by nuclear genes rf1 and rf2 is required to
restore male fertility in male-sterile cytoplasm maize (Liu et
al. , 2001); the 70 kDa heat shock protein (HSP) family has
emerged as being indispensable for male fertility (Nixon et al. ,
2017). The morphogenesis of male organs (anthers) seems to play a more
important role than the ovaries in determining floret fertility (Ji et
al. , 2010). Enhancing the morphological development of floral
anthers may be a powerful way to increase NFFs. Although several genetic
means for regulating flowering time or transforming floret fate have
been proposed (Sakuma & Schnurbusch, 2020), flowering and yield cannot
be simultaneously promoted through a single gene or biological process.
High-throughput RNA sequencing (RNA-seq) is a powerful tool for
comprehensively investigating developmental dynamics with high
sensitivity and accuracy (Yi et al. , 2019; Thiel et al. ,
2021). This provides an opportunity to clarify the gene regulatory
network of light regimens on wheat floret development, flowering
acceleration, and yield enhancement.
In this study, we aimed to dissect the complexity of assimilate
partitioning, morphological development, and transcriptional dynamics
during floret development and to clarify how the long photoperiod
supplemented with red light regimen regulates flowering and yield in
wheat. Our discoveries not only provided a guide for controlled wheat
cultivation but also revealed critical stages and candidate genes for
wheat genetics and breeding improvement during floret development.