INTRODUCTION
Understanding strategies of nutrient allocation and their underlying
mechanisms in plants adapted to phosphorus (P)-impoverished soils is an
important topic in plant physiological ecology (Lambers et al. ,
2006, Veneklaas et al. , 2012). Phosphorus-impoverished soils
limit the growth and yield of crops, pastures and forests throughout the
world (Conroy et al. , 1990, Fujita et al. , 2003, Herbert
& Fownes, 1995, Seneweera & Conroy, 1997, Thomas et al. , 2006).
Moreover, a recent meta-analysis showed that P limitation of
above-ground plant production is pervasive in natural terrestrial
ecosystems (Hou et al. , 2020). Low soil P availability is
widespread in Australia (Kooyman et al. , 2016, Viscarra Rossel &
Bui, 2016), and plants generally respond to low soil P availability by
having a low foliar P concentration (Epstein & Bloom, 2005).
Foliar P concentration is the sum of the concentrations of several major
P fractions in leaf cells including inorganic P (Pi) and various
P-containing organic compounds (i.e. nucleic acids, phospholipids and
small phosphate esters (Veneklaas et al. , 2012). Therefore,
variation in foliar P concentration among plant species or due to
environmental conditions will reflect differences in both the
concentrations of the foliar P fractions and the relative proportions
among these fractions. The allocation of P to foliar fractions is likely
related to life-history strategy, because these fractions are
functionally related to growth, reproduction, and stress tolerance.
Shifting P-allocation patterns in leaves is an important mechanism for
plants to acclimate to low soil P availability (Hidaka & Kitayama,
2011, Yan et al. , 2019). If strong P limitation occurs, plants
shift the allocation of P among foliar P fractions, and this might
increase plant fitness under the prevailing conditions (Hidaka &
Kitayama, 2011).
Chapin III & Kedrowski (1983) investigated foliar P fractions of four
Alaskan tree species and found that nucleic acid P was the largest pool
throughout the growing season, and that there was no difference in the
proportion of foliar P concentrations between different forest types.
However, these species demonstrated a relatively high foliar P
concentration (1.3–2.1 mg g-1 dry mass (DM)), so no
adaptation of the tree species to P limitation can be expected. Hidaka
& Kitayama (2009) found that plants growing on P-impoverished tropical
soils increased both leaf mass per area (LMA) and photosynthetic P-use
efficiency (PPUE) compared with plants on P-richer soil. These authors
suggested that a greater proportion of cellular P may be allocated to
metabolic P, rather than to structural P to maintain high PPUE. Yanet al. (2019) investigated foliar P fractions of three species
along a two-million-year chronosequence with a strong gradient of
available P in south-western Australia, and found that their P
allocation pattern was associated with their distribution along the
chronosequence, and concluded that the differences are likely adaptive.
How plants allocate P among foliar P fractions and exhibit adaptive
strategies to efficiently use P in two species in the same genus with
contrasting life-history strategies in extremely P-impoverished
ecosystems with a Mediterranean climate remains unclear.
The relationship between growth rate and P investment, and the
rapidly-emerging field of ecological stoichiometry have shown that
species with fast growth rates have low N:P ratios (Reef et al. ,
2010). This pattern has been explained by the Growth Rate Hypothesis
(GRH), which proposes that fast growth rates are associated with a
proportionally greater requirement for P than for N, because organisms
must allocate a disproportionately greater proportion of P to P-rich
ribosomal RNA (rRNA) to meet the protein synthesis demands needed to
support the rapid growth rates (Elser & Hamilton, 2007, Elser et
al. , 1996, Sterner & Elser, 2002). Nucleic acids have an N:P
stoichiometry of 4:1 (Reef et al. , 2010), and are a major
fraction of organic P, with RNA by far the largest proportion (Geider &
La Roche, 2002). Within the RNA pool, rRNA is the largest P fraction.
Tree species in ancient landscapes have experienced long-term low soil P
status; thus, they likely possess adaptations to P limitation.
Non-mycorrhizal Proteaceae are an important component of the vegetation
on severely P-impoverished soils in south-western Australia (Hayeset al. , 2014, Lambers et al. , 2013, Pate et al. ,
2001). Species in this family typically form cluster roots that
effectively mine soil P by releasing large amounts of
low-molecular-weight carboxylates to desorb P from soil particles (Shane
& Lambers, 2005). It is striking that mature leaves of Proteaceae
species from south-western Australia exhibit relatively fast rates of
area-based photosynthesis, despite having extremely low leaf P
concentrations (Denton et
al. , 2007, Lambers et al. , 2012, Sulpice et al. , 2014),
while leaves of P-starved crop plants tend to have slow rates of
photosynthesis per unit leaf area (Brooks et al. , 1988, Fredeenet al. , 1990, Rao et al. , 1989). Consequently, some of
these Proteaceae exhibit a very high photosynthetic P-use efficiency
(PPUE, Denton et al. , 2007, Lambers et al. , 2010, Sulpiceet al. , 2014). This high PPUE in Proteaceae from severely
P-impoverished habitats is brought about mainly by low foliar rRNA
concentrations (Sulpice et al. , 2014) and extensive replacement
of phospholipids with galactolipids and sulfolipids during leaf
development (Lambers et al. , 2012).
The slow-growing resprouter Banksia attenuata and the
faster-growing seeder B. sessilis (Pate et al. , 1991) both
produce compound cluster roots (Shane & Lambers, 2005), but have
different life histories (Shi et al. , 2020). Banksia
sessilis is a short-lived obligate seeder that occurs on shallow sand
over laterite or limestone (Hayes et al. , 2019, Pate & Bell,
1999) and allocates more biomass to cluster roots than B.
attenuata , which invests more in deep roots (Shi et al. , 2020).
This strategy enhances P mobilisation from laterite or limestone by
releasing more carboxylates and/or exuding these at a faster rate thanB. attenuata (Shi et al. , 2020). In contrast to B.
sessilis , B. attenuata is restricted to deep sand (FloraBase,
http://florabase.dpaw.wa.gov.au/) and does not grow fast and complete
its life cycle quickly (Bowen & Pate, 2017, Knox & Clarke, 2005, Pateet al. , 1990). McArthur & Wilson (1967) coined the termsr strategy and K strategy to describe selection for rapid
population growth in uncrowded populations and selection for competitive
ability in crowded populations, respectively. Over time, the meaning of
these terms has broadened (Parry, 1981), and according to the broader
context, B. sessilis is an r strategist, while B.
attenuata is a K strategist. We do not know the physiological
pattern of allocating P among foliar P fractions that allows species to
exhibit a particular life-history strategy and efficient use of P in
contrasting low-P environments. Therefore, we aimed to compare
P-allocation patterns in these two Banksia species with
contrasting life history. Thus, we measured leaf P and N concentrations,
LMA, and concentrations and proportions of P in foliar P-containing
fractions in B. attenuata and B. sessilis grown with
different soil P availability.
We hypothesised that:
1) With decreasing soil P availability, the foliar total P
concentrations of both B. attenuata and B. sessilis would
decrease.
2) Banksia sessilis , which exhibits a more opportunisticr -life strategy than B. attenuata , would have a higher
foliar NTotal : PTotal ratio and invest
more P in nucleic acids than B. attenuata when grown on the same
substrate.