Abstract
In this paper, we describe a mechanism for the transfer of nutrients from symbiotic microbes (bacteria and fungi) to host plant roots that we term the ‘rhizophagy cycle.’ In the rhizophagy cycle, microbes alternate between a root intracellular endophytic phase and a free-living soil phase. Microbes acquire soil nutrients in the free-living soil phase; nutrients are extracted through exposure to host-produced reactive oxygen in the intracellular endophytic phase. We conducted experiments on several seed-vectored microbes in several host species. We found that initially the symbiotic microbes grow on the rhizoplane in the exudate zone adjacent the root meristem. Microbes enter root tip meristem cells—locating within the periplasmic spaces between cell wall and plasma membrane. In the periplasmic spaces of root cells, microbes convert to wall-less protoplast forms. As root cells mature, microbes continue to be subjected to reactive oxygen (superoxide) produced by NADPH oxidases (NOX) on the root cell plasma membranes. Reactive oxygen degrades some of the intracellular microbes, also likely inducing electrolyte leakage from microbes—effectively extracting nutrients from microbes. Surviving bacteria in root epidermal cells trigger root hair elongation and as hairs elongate bacteria exit at the hair tips, reforming cell walls and cell shapes as microbes emerge into the rhizosphere where they may obtain additional nutrients. Precisely what nutrients are transferred through rhizophagy or how important this process is for nutrient acquisition is still unknown.
Highlights
It is widely known and accepted that most plants obtain nutrients generally through absorption of dissolved inorganic nutrients from soils [1]
Experiments using bacterial endophytes Pseudomonas spp. and Micrococcus luteus that differed in resistance to reactive oxygen degradation due to their relative capacities to produce antioxidants have suggested that bacteria that participate in the rhizophagy cycle may be matched to their particular host plants
Intracellular microbes trigger formation of root hairs on roots and they exit cells at the elongating root tips, reforming cell walls as they exit from root hairs
Summary
It is widely known and accepted that most plants obtain nutrients generally through absorption of dissolved inorganic nutrients from soils [1]. White et al [44] later documented internalization of bacteria into periplasmic spaces of root cells and their oxidative degradation within cells through use of a reactive oxygen staining technique These observations have suggested that plants are engaging in a process of microbivory in order to extract nutrients from microbes that colonize roots [45,46]. RRRoooooottt pppaaarrreeennnccchhhyyymmmaaa ccceeellllllsss ooofff aaaxxxeeennniiiccc tttooommmaaatttooo ssseeeeeedddllliiinnnggg ssshhhooowwwiiinnnggg aaabbbssseeennnccceee ooofff bbbaaacccttteeerrriiiaaa iiinnn ccceeellllllsss (((bbbaaarrr === 222555 μμμmmm;;; ssstttaaaiiinnneeeddd wwwiiittthhh 333,,,333---dddiiiaaammmiiinnnooobbbeeennnzzziiidddiiinnneee fffooollllllooowwweeeddd bbbyyyy aaaannnniiiilllliiiinnnneeee bbbblllluuuueeee)))). Lllluuutttteeeeuuuussss ((((aaaarrrrrrrrooowwwsss))) fffrrrooommm hhhaaaiiirrr tttiiipppsss (((bbbaaarrr ==== 22220000 μμμμmmmm;;;; ssstttaaaiiinnneeeddd wwwiiittthhh 333,,,333---dddiiiaaammmiiinnnooobbbeeennnzzziiidddiiinnneee fffooollllllooowwweeeddd bbbyyy aaannniiillliiinnneee bbbllluuueee))). TTTooommaattoo sseeeeddlliinngg rroooott hhaaiirr ttiipp sshhoowwiiinnnggg sssppphhheeerrriiicccaaalll LLL---fffooorrrmmmsss ooofff bbbaaacccttteeerrriiiaaa (((aaarrrrrrooowwwsss;;; bbbaaarrr ====22220000μμμμmmmm;;;; ssstttaaaiiinnneeeddd wwwiiittthhh 333,,,333---dddiiiaaammmiiinnnooobbbeeennnzzziiidddiiinnneee fffooollllllooowwweeeddd bbbyyy aaannnniiilllliiiinnnneeee bbbblllluuuueeee)))). TThhee lliitteerraattuurree ssuuggggeessttss tthhaatt ppllaannttss aalltteerr nnuummbbeerrssaannddddiivveerrssiittyyooffmmiiccrroobbeess oonn rroooott ssuurrffaacceess aanndd iinn tthhee rrhhiizzoosspphheerree tthhrroouugghh sseeccrreettiioonn ooff eexxuuddaatteess [[6600]]. It seems probable that plants would not be internalizing and degrading symbiotic microbes unless critical nutrients were being obtained from consumption of those microbes
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