Ferns preferentially use the daily carbon assimilated to
the synthesis of secondary rather than primary metabolites
In order to better understand the metabolic differences between ferns
and angiosperms, we performed an unprecedented LC-MS analysis of ferns
leaves, which, combined with our previous published GC-MS-based
metabolite profiling analysis (Lima et al. 2019), provided a
clear depiction both regarding the metabolic differences among ferns and
angiosperms and metabolic aspects underpinning the regulation of
stomatal speediness. Multivariate analyses indicate that ferns and
angiosperms differ substantially at metabolic level, as evidenced by
their separation following HCA, orthoPLSDA and PCA. The LC-MS-based
metabolic fingerprinting analysis further showed that several features
are solely found in ferns (Figure 4), indicating a higher chemical
diversity, compared to the angiosperms species studied here.
Furthermore, several features found in both plant groups have higher
level in ferns than angiosperms throughout the diel course (Figure 6),
suggesting that ferns have a higher accumulation of secondary
metabolites than angiosperms. This idea is further supported by the fact
that amino acids precursors of secondary metabolism such as
phenylalanine and tryptophan are present at higher levels in ferns than
angiosperms throughout the diel course, while the majority of sugars and
other amino acids have higher levels, throughout the diel course, in
angiosperms, when compared to ferns (Lima et al. 2019). These
results strongly indicate that ferns prioritize carbon allocation
towards secondary rather than primary metabolism. Given the role of
secondary metabolites for plant defense against (a)biotic stresses
(Martins et al. 2014; Tohge et al. 2016; Austen et
al. 2019; Li et al. 2021) and the evidence indicating that ferns
have greater tolerance to different stress conditions, when compared to
angiosperms (Proctor & Tuba 2002; C.H et al. 2017; Salachna &
Piechocki 2020), it seems likely that the higher allocation of carbons
toward the secondary metabolism could be a mechanism to improve stress
tolerance in ferns, at expenses of reduced growth (Figure 9). These
results contribute to answer the elusive question as to why the growth
of ferns is slow and sheds light on the challenge that plant breeding
programs face to produce stress tolerant genotypes in the absence of a
major yield penalty.