Loss of LaMATE impairs isoflavonoid release from cluster roots of phosphorus‐deficient white lupin

Abstract

White lupin (Lupinus albus L.) forms brush-like root structures called cluster roots under phosphorus-deficient conditions. Clusters secrete citrate and other organic compounds to mobilize sparingly soluble soil phosphates. In the context of aluminum toxicity tolerance mechanisms in other species, citrate is released via a subgroup of MATE/DTX proteins (multidrug and toxic compound extrusion/detoxification). White lupin contains 56 MATE/DTX genes. Many of these are closely related to gene orthologs with known substrates in other species. LaMATE is a marker gene for functional, mature clusters and is, together with its close homolog LaMATE3, a candidate for the citrate release.Both were highest expressed in mature clusters and when expressed in oocytes, induced inward-rectifying currents that were likely carried by endogenous channels.No citrate efflux was associated with LaMATE and LaMATE3 expression in oocytes. Furthermore, citrate secretion was largely unaffected in P-deficient composite mutant plants with genome-edited or RNAi-silenced LaMATE in roots. Moderately lower concentrations of citrate and malate in the root tissue and consequently less organic acid anion secretion and lower malate in the xylem sap were identified. Interestingly, however, less genistein was consistently found in mutant exudates, opening the possibility that LaMATE is involved in isoflavonoid release.

Improving phosphorus acquisition efficiency through modification of root growth responses to phosphate starvation in legumes

“…Similarly, LaALMT1 is also characterized to be the plasma membrane-localized malate transporter in white lupin (Zhou et al, 2020). In addition, several genes encoding citrate transporters have also been reported in legumes, such as VuMATE in rice bean (Vigna umbellata) and LaMATE1/3 in white lupin, all of which are induced by P deficiency (Wang et al, 2013;Loṕez-Arredondo et al, 2014;Zhou et al, 2021). For instance, LaMATE1/3 exhibit the highest expression in mature cluster root under low-P conditions; mediating citrate transport when LaMATE1/3 are expressed in oocytes, suggesting the role for LaMATE1/3 in regulating citrate transport during low P stress (Zhou et al, 2021).…”

“…In addition, several genes encoding citrate transporters have also been reported in legumes, such as VuMATE in rice bean (Vigna umbellata) and LaMATE1/3 in white lupin, all of which are induced by P deficiency (Wang et al, 2013;Loṕez-Arredondo et al, 2014;Zhou et al, 2021). For instance, LaMATE1/3 exhibit the highest expression in mature cluster root under low-P conditions; mediating citrate transport when LaMATE1/3 are expressed in oocytes, suggesting the role for LaMATE1/3 in regulating citrate transport during low P stress (Zhou et al, 2021). In addition, secreting protons by legume root can acidify the rhizosphere soil, thereby improving the bioavailability of insoluble P (Kouas et al, 2009).…”

Harnessing belowground processes for sustainable intensification of agricultural systems

“…MATE? 1 Numerous species forming mycorrhizal symbiosis with Glomus (AM) , Gigaspora (AM) , Suillus bovinus (EM) Cesco et al ( 2012 and references therin) Flavonoids—Flavanones: Hesperetin, naringenin Phenylpropanoid biosynthesis & glycolysis Stimulation of spore germination Flavonoids—Isoflavonoids: Daidzein, genistein Phenylpropanoid biosynthesis & glycolysis Stimulation of mycorrhizal colonization & spore germination Flavonoids: Izoliquiritigenin, liquiritigenin, daidzein, formomonetin, apigenin, afrormosin, medicarpin, vestitone Phenylpropanoid biosynthesis & glycolysis Triggering of root infection by rhizobial strains & nodule formation 4 ABCG-type Legumes, Medicaco truncatula Banasiak et al ( 2013 ) Flavonoids—Isoflavonoids: Genistein Phenylpropanoid biosynthesis & glycolysis Triggering nodule infection Induction of fungal sporulation leading to vegetative growth reducing exudate consumption LaMATE2 Lupinus albus Biała-Leonhard et al ( 2021 ); Weisskopf et al ( 2006 ); Zhou et al ( 2021 ) Terpenoids—Diterpene: Abietic acid MEP pathway Stimulation of spore germination Unknown Pinus sylvestris Fries et al ( 1987 ) (b) Pathogen interaction & toxicity response Benzoxazinoids (BX): 2,4-Dihydroxy-7-methoxy-1,4- benzoxazin-3-one glucose ( DIMBOA-Glc), DIMBOA, N–O-methylated DIMBOA-Glc (HDMBOA-Glc) Amino acid metabolism, tryptophan biosynthesis, indole metabolism Inhibition of host recognition and virulence of pathogenic Agrobacterium tumefaciens16 Unknown 2 …”

Global Identification of White Lupin lncRNAs Reveals Their Role in Cluster Roots under Phosphorus Deficiency

“…White lupin ( Lupinus albus ) has been illuminated as a model crop to disclose root physiology and adaptive responses to P deficiency [ 39 ], and develop cluster roots (CRs) in response to P deficiency [ 39 , 40 ]. Cluster roots enhance Pi acquisition and exudate a huge amount of carbon metabolites such as citrate and malate [ 40 , 41 ].…”

“…White lupin ( Lupinus albus ) has been illuminated as a model crop to disclose root physiology and adaptive responses to P deficiency [ 39 ], and develop cluster roots (CRs) in response to P deficiency [ 39 , 40 ]. Cluster roots enhance Pi acquisition and exudate a huge amount of carbon metabolites such as citrate and malate [ 40 , 41 ]. Citrate exuded upon P deficiency is known to play important role in mobilizing organic P complexes available in the soil [ 42 ], and provides evidence in support of the involvement of organic anions in P solubilization.…”