Genetic regulation of longevity in flowering plants

Plant genes encoding a group of nuclear proteins link flowering genes and a
flowering-promoting hormone pathway to promote longevity

By Pengxin Yu

Plants have very diverse life histories. For the flowering plants, one of the ways to
classify them is by their life span: plants that die after flowering are called annuals,
since they have only a single growing season, while the ones that do not die and
repeat flowering in consecutive years are termed perennials. For example, the model
organism Arabidopsis thaliana Columbia (Col-0) accession is a summer annual with
monocarpic growth, because it flowers rapidly under long days. In contrast, some
relatives of A. thaliana such as Arabidopsis lyrata and Arabis alpina are perennials
(polycarpic). These different reproductive strategies are based on the behaviours of
meristems, consisting of the stem cells. In A. thaliana all shoot meristems flower
irreversibly when receiving the appropriate induction signals, while the perennials
only flower on some meristems and preserve others as vegetative for the next year
(Albani & Coupland, 2010). Thus, identifying pathways that integrate signals into the
flowering circuits in the meristems becomes an importance task.

On page 368 of this issue, Karami et al. (2020) uncovered a new role for the
Arabidopsis AT-HOOK MOTIF NUCLEAR LOCALIZED 15 (AHL15) and other AHL
clade-A genes in suppressing axillary meristem (AM) maturation and promoting
longevity. AMs are regions on the side of the plant stem that develop into future side
shoots and potentially inflorescences, and staining confirmed AHL15 expression in
the AMs. The ahl15 loss-of-function A. thaliana mutant plants flower at the same
time as the wildtype, but after flowering, they produce fewer rosette leaves from the
rosette AMs, and fewer cauline leaves, flowers, and fruits from the aerial AMs on the
cauline branches. On the other hand, overexpression of AHL15, four other AHL
family members, and AHL15 orthologues from Brassica and Medicago all resulted in
more leaves and delayed flowering. Since flower development first occur at the shoot
tip, this suggests that AHL genes might affect both shoot apical meristem (SAM) and
AM maturation.

Karami et al. found that under short day (SD) conditions, ahl15 mutant A. thaliana die
after flowering, while wildtype and ahl15 pAHL15:AHL15 plants continue to grow
after flowering due to new rosette leave development on the young lateral branches.
As wildtype A. thaliana Col-0 dies within 2 months under long day (LD) conditions,
AHL15 was suspected to be implicated in this day length sensitivity. Indeed, AHL15
expression is strongly upregulated under SD compared to LD conditions. Using
different promoters, the authors uncoupled AHL15 from the day length regulation of
flowering time, resulting in AHL15 overexpressors, when grown under LD conditions,
have unaltered flowering time, but produce more leaves and showed multiple rounds
of vegetative development after flowering and seeding- a phenotype similar to that of
A. alpina, only that here the AMs do not show dormancy. Overexpressing AHL15 in
the annual tobacco plants led to the same conclusion that AHL15 promote longevity.

SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1) and FRUITFULL

(FUL) are important flowering regulators, and their loss-of-function A. thaliana
mutants shows polycarpic-like growth (Melzer et al., 2008). Here, genetic crosses,
expression analyses and DNA binding assays were used to demonstrate that AHL15 is
repressed by SOC1 and FUL during flowering. Additionally, signals from the
hormone gibberellin (GA) were previously reported to integrate into the SOC1-FUL
pathway (Porri et al., 2014), but in this study, AHL15 was found to be a suppressor of
GA biosynthesis. Therefore, AHL15 is placed between the SOC1/FUL and GA
pathways in A. thaliana AM maturation (Fig.1, left). This is in direct contrast to A.
alpina, where another flowering suppressor gene PERPETUAL FLOWERING1
(PEP1) functions upstream of both SOC1/FUL and GA pathways to control its
polycarpic habit (Albani et al., 2011; Hyun et al., 2016, 2019; Tilmes et al., 2019)
(Fig.1, right). It was suggested that PEP1 interactions are conserved in A. thaliana,
and it is the integration of various cues that underpins the differential annual/perennial
flowering responses (Hyun et al., 2019). Since the AHL gene family also exist in A.
lyrata (Karami et al., 2020), it will be interesting to investigate whether its members
such as AHL15 function through the same pathways but result in perennialism.

Flowering on old meristems during vernalization

PEP1

Figure 1. AHL15 and PEP1 link SOC1/FUL and GA pathway to control meristem maturation and floral induction. Left:
AHL15 in A. thaliana is a repressor of axillary meristem maturation. Figure adapted from Karami et al. (2020). Right:
PEP1 in Arabis alpina represses flowering through a pathway that integrate both vernalization and aging cues (not
shown here). Blunt-ending lines indicate repression, arrows indicate promotion.

The results of Karami et al. revealed a novel role for AHL clade-A genes in promoting
plant longevity, and exemplified how flowering response occurs by integrating signals
from different pathways, eventually affecting reproductive strategy and lifespan.
Karami et al. also found that AHL genes shows differential expression between A.
thaliana and A. lyrata, suggesting that life history divergence might not necessarily
need novel genes. Further research is need to shed light on the genetic interactions of
AHL with the vernalization sensor PEP1 and the signal integrators SQUAMOSA
PROMOTER BINDING PROTEIN LIKE15 (SPL15) and FLOWERING LOCUS T
(FT) (Hyun et al., 2019). Additionally, the molecular mode of action of AHL proteins
 such as DNA binding and chromatin remodeling will be worth exploring.

References
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