Effects of root morphology, respiration and carboxylate exudation on carbon economy in two non‐mycorrhizal lupines under phosphorus deficiency

Abstract

Under phosphorus (P) deficiency, Lupinus albus develops cluster roots that allow efficient P acquisition, while L. angustifolius without cluster roots also grows well. Both species are non‐mycorrhizal. We quantitatively examined the carbon budgets to investigate the different strategies of these species. Biomass allocation, respiratory rates, protein amounts and carboxylate exudation rates were examined in hydroponically‐grown plants treated with low (1 μM; P1) or high (100 μM; P100) P. At P1, L. albus formed cluster roots, and L. angustifolius increased biomass allocation to the roots. The respiratory rates of the roots were faster in L. albus than in L. angustifolius. The protein amounts of the non‐phosphorylating alternative oxidase and uncoupling protein were greater in the cluster roots of L. albus at P1 than in the roots at P100, but similar between the P treatments in L. angustifolius roots. At P1, L. albus exuded carboxylates at a faster rate than L. angustifolius. The carbon budgets at P1 were surprisingly similar between the two species, which is attributed to the contrasting root growth and development strategies. L. albus developed cluster roots with rapid respiratory and carboxylate exudation rates, while L. angustifolius developed a larger root system with slow respiratory and exudation rates.

A starting guide to root ecology: strengthening ecological concepts and standardising root classification, sampling, processing and trait measurements

“…However, Funayama‐Noguchi et al . ( 2020 ) recently reported that the overall expenditure of C for RR S remained similar in two Lupinus spp. irrespective of the presence of cluster roots, pointing towards a tight regulation of whole root system C consumption across different entities via closely controlled metabolic pathways.…”

“…As RR S strongly differs among root orders and the relative proportion of distinct root orders differs among species, RR of entire root systems cannot be inferred directly from RR S of specific root orders; in species comparisons, researchers should consider on what root entity RR S was measured (Rewald et al, 2014). However, Funayama- Noguchi et al (2020) recently reported that the overall expenditure of C for RR S remained similar in two Lupinus spp. irrespective of the presence of cluster roots, pointing towards a tight regulation of whole root system C consumption across different entities via closely controlled metabolic pathways.…”

“…While the ATP yield of fermentation is markedly less then that of aerobic respiration, ATP production efficiency under aerobic conditions can depend on the involvement on different metabolic pathways, such as alternative oxidase and uncoupling proteins, beside oxidative phosphorylation (e.g. Funayama‐Noguchi et al ., 2020 ). See Plaxton & Podestá ( 2006 ) and Del‐Saz & Ribas‐Carbo ( 2018 ) for reviews on the (eco‐)physiology of plant respiration.…”

“…The RR S depends on three major energy‐requiring processes: (1) ion uptake (mostly N) and mobilisation (via exudation), (2) growth and defence, and (3) maintenance of living cells (Van der Werf et al ., 1994 ). Root mycorrhizal symbionts and bacteria on the rhizoplane and in intercellular spaces can contribute to measured RR S (Nielsen et al ., 1998 ; Bulgarelli et al ., 2012 ), while CO 2 fixation in the roots by phosphoenolpyruvate carboxylase and exudation of carboxylates would lower respiratory CO 2 release (Funayama‐Noguchi et al ., 2020 ). The specific C and O 2 costs per unit of ion uptake or root growth roughly indicate the C‐use and O 2 ‐use efficiencies, therefore RR S is one important variable determining the roots’ foraging/uptake efficiency (George et al ., 2003 ; Lynch, 2015 ).…”

Growth temperature affects O2 consumption rates and plasticity of respiratory flux to support shoot growth at various growth temperatures

“…After the measurement of O 2 consumption rates, we quantified AOX and subunit II of COX (COXII) in the samples according to the method of Funayama‐Noguchi et al (2021), except that we detected chemiluminescent signals using a luminescent image analyser (WSE‐6100, ATTO) and quantified them using CS Analyzer4 (ATTO). We estimated the relative amount of each protein on the leaf dry weight basis using the data of the relative amount of protein on the total protein basis and the data of N content on the dry weight basis.…”