4.1 Phloem ontogeny and lianescence
During stem ontogeny, lianas that rely exclusively on twining for
climbing, such as A. scandens , transition abruptly from
self-supporting branches, known as searchers, to stiffer ones that grow
in close contact with a solid support. In A. scandens , the
photosynthetic, non-lignified searcher branches contain more phloem than
xylem tissue, likely because the immature leaves have little demands of
water, but a significant need of carbohydrates. This limited xylem
implies that pith turgor might be the major contributor to the
mechanical stability of searcher branches, as reported in other twining
vines (Isnard & Silk, 2009). Morphologically, the tube-like primary
sieve elements that dominated the vasculature of searchers suggested
lack of lateral transport, but directional sap flow toward growing
branch tips. Chemically, sieve tube walls of searcher stems were
composed of a galacturonan-rich pectin, which has been described in a
handful of species such as in leaves of Beta vulgaris (Torode et
al., 2018), or in the seasonally renovated sieve tubes of Populus(Ray & Savage, 2020). These previous works strongly emphasized that the
chemistry of the cell walls connect with mechanics of the sieve tube
wall (Torode et al., 2018). Thus, this wall related epitope may
contribute to the flexibility of searcher branches, and it may also be
present in sieve tubes in the secondary phloem. Nevertheless, its
presence in the primary sieve tubes of A. scandens demonstrates
that this distinctive pectin is found in the sieve tubes of angiosperms
with different life histories, growth habits, and phylogenetic
backgrounds.
Despite the conservation of diameter in rigid twining stems, leaf area
increased and reached full expansion. Basipetally, the phloem in the
twining stems acquired a lobed topology, and the sieve tubes an
increasing number of plate connections, features that suggest an
increase in transport efficiency under torsion. In fact, the complex
division patterns (i.e. tangential longitudinal) of the secondary phloem
of A. scandens were evaluated in detail about 50 years ago
(Srivastava, 1970), and differed from axial longitudinal divisions
observed in other woody angiosperms, suggesting a correlation with the
helical gyres of the lianoid growth habit. In line with these
observations, we further noticed that, in areas of high rotation at the
base of the stems, the sieve tube elements were shorter (Silk &
Holbrook, 2005), reinforcing the idea that the vascular cambium activity
is influenced by the mechanics of lianoid stems (Pace et al., 2015,
2018). How this mechanical (un)stability affects function has been
studied for the lianoid xylem, which enhances hydraulic efficiency
through more volumetric vessels despite the strong torsional pressures
such as twisting and bending (Putz & Holbrook, 1992; Gentry, 1991;
Speck & Rowe, 1999; Rowe et al., 2006). Our measurements revealed that
sieve tube geometries are more conserved across species, and A.
scandens displays radii of sieve elements (7-13 µm), which fall within
parameters measured in the slender stems of Ipomoea nil (10-20
µm) (Knoblauch et al., 2016), or the trunks of canopy dominant trees
(6-24 µm) (Liesche et al., 2017; Savage et al., 2017). The radii of the
sieve tube elements increase basipetally at long distances, as observed
in tall trees (Jensen et al., 2012, Savage et al., 2017). Strikingly
though, the average sieve plate pore size of A. scandens (0.20µm
radius) was smaller than in stems of other species, and varied little
axially. Because pore size is the factor that affects phloem hydraulics
the most, A. scandens has high phloem resistance in the stem,
compared with other species (Liesche et al., 2017; Savage et al., 2017;
Clerx et al., 2020; Barceló-Anguiano et al., 2021a), but within the
parameters observed in other Austrobaileyales of the understory (Losada
& Holbrook, 2019). To compensate for the small sieve plate pore size,
the secondary phloem of A. scandens has an unusually high number
of sieve plates along the tangential walls of phloem conduits. Compound
sieve plates have been correlated with growth form in height across
woody species that reach the forest crowns (Pace et al., 2015; Knoblauch
et al., 2016; Liesche et al., 2017; Savage et al., 2017; Losada &
Holbrook, 2019; Clerx et al., 2020; Barceló-Anguiano et al., 2021a,b).
Reasons behind the particular phloem morphology of A. scandens(lobed arrangement in cross sections, tapered tubes with angled plates
and different lengths) may reflect life history traits associated with
the liana growth form, such as the imbalance of carbon allocation
between the leaf canopy and stem tissues. Thus, a reduced number of
below-canopy sink tissues and higher canopy sinks favor a more
functional phloem aboveground, whereas in the understory, the mechanics
of twining constrains the morpho-functional aspects of phloem (for
example, the length of the sieve tubes).