Regulation of Root Traits for Internal Aeration and Tolerance to Soil Waterlogging-Flooding Stress

Root acquisition of water and nutrients is essential for plant growth and crop productivity (Lynch, 2015). An improved understanding of root system development and functioning, to identify root traits contributing to crop yields in various scenarios, is a research frontier that might enable a second Green Revolution needed to sustain world food security (Lynch, 2007). Roots are challenged by various abiotic and biotic constraints in soils, with water status of too little or too much being a major factor resulting in plant stress. Changing rainfall patterns have resulted in increased flood events in many regions, so that the development of flood-tolerant crops is a priority (Bailey-Serres et al., 2012). Water-saturated soils (i.e. waterlogged soils) are often anoxic, so that roots of poorly adapted species suffer oxygen deficiency that reduces respiration and results in a severe energy crisis, whereas well-adapted wetland species can thrive (Bailey-Serres and Voesenek, 2008). The detrimental impact on upland crops of soil waterlogging can be substantial (e.g. wheat [Triticum aestivum]; Setter and Waters, 2003; Herzog et al., 2016). Root morphological and anatomical traits determine root growth and functioning in anoxic waterlogged soils. An increased number of newly emerged adventitious roots can compensate, at least partially, for the growth inhibition or even death of distal portions of roots present when waterlogging occurs (Jackson and Drew, 1984). Many plant species produce adventitious roots (Visser and Voesenek, 2004), with some emerging into the soil, others along the soil surface, and during deeper floods some even grow into the water column; the latter are referred to as aquatic adventitious roots. The formation of aerenchyma (Fig. 1), the induction of a barrier to restrict radial oxygen loss (ROL) to the soil (Fig. 1), and the rate of respiratory consumption along roots together largely determine the internal oxygen supply along roots and, thus, the energy status and growth in anoxic waterlogged soils (Armstrong, 1979). Internal oxygen transport along roots via aerenchyma and enhancement of oxygen diffusion to the root tip by a barrier to ROL in the basal root zones. A, Scheme of aerenchyma and spatial patterns of ROL along roots of rice. Rice roots constitutively form some aerenchyma in well-drained soil but not a tight ROL barrier, so that ROL from basal zones is substantial. During waterlogging, roots develop more aerenchyma and a tight barrier to ROL is induced. OPR, outer part of the root; ep, epidermis; hy, hypodermis/exodermis; sc, sclerenchyma; co, cortex; ae, aerenchyma. Bar = 100 μm. B, ROL from rice adventitious roots was visualized by staining with Methylene Blue in an oxygen-free medium. Blue color indicates oxygen, which diffused outward from the root surface. Cross sections are from just behind the tip (apex), middle, and basal parts of adventitious roots of rice grown under stagnant conditions (oxygen-free rooting medium, shoot in air). Lysigenous aerenchyma is indicated by arrowheads. Bar in the left image (Methylene Blue staining) = 10 mm; bars in the right images (root cross sections) = 100 µm. C, Percentage of aerenchyma of root cross-sectional area and profile of ROL along adventitious roots under stagnant conditions. Nine-day-old aerobically grown rice seedlings were further grown under stagnant conditions for 14 d, and 110- to 130-mm-long adventitious roots, which had emerged under stagnant conditions, were subjected to the experiments. Values are means ± sd (n = 3). Aerenchyma started to form between 10 and 20 mm behind the tip, and the amount of aerenchyma increased toward the root base. Tissue porosity resulting from cubic cell packing would facilitate oxygen diffusion in the tip region. By contrast, the ROL was greatest near the root tip and least in the basal zones due to the induction of a tight barrier to ROL in the outer part of the root; the ROL barrier starts to form at 20 to 30 mm behind the root tip. These two traits facilitate the internal oxygen diffusion from shoots to root tips of wetland plants (e.g. rice) in waterlogged soil. Photographs and unpublished data are from T. Yamauchi and M. Nakazono. Aerenchyma provides an internal path for low-resistance gas-phase diffusion of oxygen into and along roots (Fig. 1A). Root growth into anoxic waterlogged soils depends upon the distance to which adequate oxygen can reach to sustain the respiratory demands of the root apex as it grows farther away from the shoot base and the source of the oxygen (Armstrong, 1979). Thus, roots of greater gas-filled volume (i.e. greater porosity) can achieve longer lengths in waterlogged soil than roots of low porosity (Armstrong, 1979; Justin and Armstrong, 1987). Importantly, oxygen within the root aerenchyma not only diffuses in the longitudinal direction to the root tip; some of the oxygen is consumed by the root cells and some is also lost radially (i.e. ROL) to the rhizosphere (Fig. 1A). Many wetland plants, including rice (Oryza sativa), develop a barrier to ROL in the basal zone of roots, so that ROL is restricted and oxygen diffusion is promoted along the aerenchyma toward the root tip (Fig. 1A; Armstrong, 1979; Colmer, 2003b). This Update focuses on the root morphological and anatomical traits determining oxygen supply to the distal tips of roots in waterlogged soils and the regulation of these traits during acclimation to waterlogging-flooding stress. Metabolic acclimations to hypoxia (low oxygen) and anoxia (zero oxygen) also are important for plants during waterlogging-flooding stress, and these are considered elsewhere (Gibbs and Greenway, 2003; Greenway and Gibbs, 2003; Bailey-Serres and Voesenek, 2008; Voesenek and Bailey-Serres, 2015). Recent findings on aerenchyma formation, root ROL barrier induction, and the functioning of aquatic adventitious roots are summarized to highlight advances in knowledge of the signaling pathways underpinning root plasticity to acclimate to waterlogging-flooding events. The use of laser microdissection to enable transcript profiling of specific tissues has delivered insights into ethylene and reactive oxygen species (ROS) signaling pathways for aerenchyma formation in the root cortex and into suberin biosynthesis for ROL barrier formation in the root hypodermis/exodermis. Moreover, quantitative trait locus (QTL) analysis using mapping populations of barley (Hordeum vulgare) and cucumber (Cucumis sativus), and most notably produced from wide hybridization of a wetland wild relative Zea nicaraguensis with the upland crop maize (Zea mays ssp. mays), have yielded genetic information on important traits of aerenchyma formation, ROL barrier formation, and adventitious rooting. Aerenchyma forms in primary tissues (primary aerenchyma) and in secondary tissues (secondary aerenchyma; Yamauchi et al., 2013; Takahashi et al., 2014). In primary aerenchyma is further into aerenchyma and aerenchyma and Armstrong, 1987). Lysigenous aerenchyma is by the death and of cells in roots (Fig. or cells in whereas aerenchyma in roots is by the of of cells of cells and Armstrong, et al., Takahashi et al., 2014). Lysigenous aerenchyma formation has at the whereas aerenchyma formation has so in Update on resulting in which is the in roots of rice and Lysigenous aerenchyma forms in roots of a of including many important plants as In aerenchyma forms not only in roots but also in the and and 2008). In roots of some wetland plants, as aerenchyma is constitutively under well-drained soil conditions, and formation is further upon soil waterlogging (Fig. 1A). The and latter are as and aerenchyma formation, and Voesenek, Roots of plants, as maize and form aerenchyma under waterlogged soil conditions but not form aerenchyma under well-drained soil conditions and Voesenek, aerenchyma formation to waterlogging as for nicaraguensis with a of aerenchyma formation and the death of root cells root is in maize and barley under or when (e.g. or et al., The death of root cells reduces the respiratory and of the root of to sustain some root growth under or conditions (Lynch, et al., The formation of aerenchyma the oxygen status of roots, but is a diffusion along the of the root so that oxygen with distance from the (Fig. 1A; Armstrong, 1979). In to longitudinal oxygen along the root radial profiling of oxygen also in oxygen between tissues et al., et al., In radial oxygen of oxygen from the cortex from the when oxygen is present with oxygen in the cortex via aerenchyma) and oxygen in the which also can have a respiratory or even in the tissues of roots in a (Gibbs et al., and also in roots on the internal of oxygen via aerenchyma when the of oxygen of the shoots was to 10 et al., anoxia can impact transport (e.g. in maize et al., and barley et al., The of these findings are that a can be of for waterlogging as roots with a diffusion path into the and greater cortex would anoxia oxygen to than for roots with a and 1987). aerenchyma formation cell death which is by ethylene et al., in the of the ethylene can the of specific cell (i.e. cells in shoots or cells in and, only some of these cells in a Recent and waterlogged conditions, ethylene in roots due to to the rhizosphere and the enhancement of ethylene biosynthesis in the roots (Fig. Voesenek and 2013; and Voesenek, 2015). is produced from in two by the of and (Fig. The oxygen for the of to The of for oxygen is to in for from roots and in of the to oxygen of ethylene is for adventitious roots of in which it was in anoxia with whereas ethylene was at oxygen to be that in with oxygen (Jackson et al., of the signaling for aerenchyma formation in rice roots, on findings by Yamauchi et waterlogged conditions, the of oxygen from the into soil is by restricted which results in low oxygen whereas ethylene in roots are due to the restricted of the the ethylene and are increased in and the resulting in would ethylene biosynthesis in roots, that some oxygen is to due to the restricted further ethylene in roots. In the biosynthesis of is under stagnant conditions, and are to have a in in rice roots by an as In root ethylene the of a the respiratory which oxygen to the in the from the is in roots. is and by as and The by (e.g. results in an in in the In of the of which as a to in the root the increased of and aerenchyma formation in the root Roots of (i.e. plants form aerenchyma under conditions water and nutrients are 2015). The of soil waterlogging, in anoxia and the tips and distal parts of these roots of low gas-filled porosity aerenchyma can form et al., 2014). By contrast, aerenchyma is constitutively in roots of many wetland plants (Armstrong, 1979; and 2008; and Voesenek, thus, some oxygen is present farther along roots the of waterlogging so that respiration can which would aerenchyma formation might not only be for the of waterlogging aerenchyma but the internal also would oxygen for ethylene needed to the aerenchyma a greater amount of aerenchyma also would facilitate some of ethylene from the roots (Visser and would only impact aerenchyma formation ethylene the but increased ethylene and aerenchyma formation in rice roots under conditions et al., that a low of is rate for ethylene biosynthesis in these roots. the the of ethylene in roots of rice and maize the of a in rice roots than in maize roots under conditions was with a more of ethylene in rice roots than in maize roots the of conditions et al., 2016). In rice roots, the of and are most increased under stagnant conditions et al., 2015). conditions, and when elsewhere in to a that the in (low oxygen and ethylene and in waterlogged soils et al., Recent of a rice have a between or more and ethylene The rice has a in the an the of have not of the major suberin from et al., The induction of is in roots, in which of and (i.e. and were than in the roots et al., 2015). and aerenchyma formation in roots. of rice seedlings with the (i.e. ethylene and aerenchyma formation in adventitious roots under stagnant conditions et al., 2015). These results that are or in ethylene biosynthesis and, thus, to aerenchyma formation in rice roots when in stagnant conditions (Fig. the regulation of aerenchyma formation in roots understanding is much for the regulation of aerenchyma formation under conditions. and that the ethylene aerenchyma formation in rice roots grown on an This that ethylene is not only in aerenchyma formation but also in aerenchyma This was by Yamauchi et that also aerenchyma formation in rice roots in The formation of some aerenchyma even when roots were with and Yamauchi et al., that aerenchyma formation in rice roots is by an as as the the of The during aerenchyma formation in roots et al., Yamauchi et al., and shoots et al., et al., a plant of oxygen to (Fig. analysis using tissues of rice roots that a is most in cells under stagnant conditions et al., of the in which was by reduces and aerenchyma formation et al., In to signaling also is in for aerenchyma formation et al., et al., In rice roots, two of and are in cells of roots under stagnant conditions et al., or when or is with in et al., This that in rice roots is of (Fig. The ethylene the of not the of or and reduces aerenchyma formation under stagnant conditions et al., that of by ethylene is for the during aerenchyma formation in rice roots. it to be ethylene the in (e.g. by from under conditions. In maize roots, of the the of is during aerenchyma formation under waterlogged conditions, and is by et al., and only a of species have that the of aerenchyma formation an and signaling of cells is a in roots of plants in the transcript in roots of rice and maize under stagnant and waterlogged conditions, not only in the cells but also in root transcript are in cells et al., Yamauchi et al., The in to with a that as a being a factor (Fig. In maize roots, the of a in the but it is in the cells and in the outer cell of the roots under waterlogged conditions et al., Yamauchi et al., in rice roots are in the outer cell of the roots et al., the of and also is under stagnant conditions et al., These findings that in of the determine the of cells for in roots during aerenchyma when are in the cells of rice aerenchyma formation is by the of et al., and two which are for the and et al., In adventitious roots of the of some are than of et al., By to roots, in the of are than et al., a major in in roots, whereas in it that the the major analysis of is to the cell of and cell death during aerenchyma formation in roots of the analysis of aerenchyma formation under (i.e. conditions using a or mapping produced by maize and a wild relative that than maize to soil waterlogging (Fig. for aerenchyma formation in two on and on and and et al., 2016). In a major for aerenchyma formation in roots that of the is on for a produced from and et al., 2016). analysis of aerenchyma formation in roots also has using a from barley and et al., a major for aerenchyma formation in roots was from the which also on and at the or to the for trait in the et al., Moreover, the for aerenchyma formation on to the area as a major for waterlogging from the et al., are needed to identify the these for root aerenchyma formation and to the pathways to the of these of nicaraguensis and ROL barrier formation in roots as as in a in A, in the is in nicaraguensis than in maize of and and C, of ROL along roots of and the which the locus for ROL barrier formation of nicaraguensis in the genetic of under stagnant conditions rooting medium, shoot in air). B, ROL from adventitious roots visualized by Methylene Blue staining in an oxygen-free medium. Blue color indicates oxygen that has diffused outward from roots. = 10 C, of using a oxygen along adventitious roots in an oxygen-free with the shoot in Values are means ± sd (n = The ROL was low from the basal zones of roots of nicaraguensis and due to the induction of a tight ROL barrier, which starts to form at 20 to mm behind the that the of the ROL occurs from roots of nicaraguensis and are not between the Methylene Blue staining and the using oxygen as can for of plants, but in the basal had low by contrast, not form a tight ROL barrier in roots. The root porosity of nicaraguensis than of is to to the ROL in the root tips of Photographs in and data in are from et with from Roots of many wetland plants a barrier to restrict ROL from basal in the longitudinal diffusion of oxygen along the aerenchyma toward the root tip (Fig. Armstrong, 1979; Colmer, 2003b). to radial oxygen diffusion from suberin in cell (e.g. in wetland et al., et al., et al., 2008; et al., in the outer cell also oxygen (Armstrong, 1979; et al., et al., 2008). The ROL barrier was in roots of by radial oxygen which a in oxygen the in the basal portions (i.e. 100 mm behind the root of the roots, the to radial together with oxygen consumption in the outer cell resulted in ROL the oxygen within the aerenchyma and the to the anoxic et al., The ROL barrier, in to oxygen also the of soil (e.g. into roots in waterlogged soils (Armstrong, 1979; and Armstrong, Importantly, the greater the ROL barrier cells not to the of nutrients (e.g. et al., and might have for water et al., et al., data on these are and roots with tight ROL be for and for radial The quantitative spatial patterns of ROL from roots of which a barrier to were (Armstrong, The root ROL barrier was to in wetland and the for root was (Armstrong, 1979). The that the rice root ROL barrier is to growth conditions, being or only in conditions but with a tight ROL barrier in roots when in stagnant or waterlogged conditions et al., Colmer, in root the radial of the outer part of the root is to conditions in rice and also in roots of some wetland whereas a root ROL barrier forms constitutively in wetland species et al., Colmer, 2003b). The signaling for root ROL barrier induction to be the formation of aerenchyma (Fig. and but ethylene not the root ROL barrier in rice et al., under stagnant conditions ROL barrier development but low oxygen using is not to ROL barrier was the of low oxygen and ethylene et al., also can to in waterlogged soils et al., but not barrier formation in rice et al., induction is in roots but in longer roots, that root the ROL barrier et al., et al., induction within the upon of a root system to stagnant conditions et al., cell develop during the of ROL barrier formation et al., analysis using tissues of the outer cell of rice roots that many in suberin biosynthesis not were during ROL barrier formation in rice et al., Moreover, and in the rice roots a ROL barrier, that is for the biosynthesis of in for suberin biosynthesis et al., 2014). various in waterlogged soils resulting from the of can a ROL barrier in roots of wetland these and Armstrong, et al., and and Armstrong, et al., 2014). research is needed to the signaling events and regulation of root ROL barrier An root ROL barrier forms in some wild of upland as et al., et al., 2003; et al., and nicaraguensis et al., et al., The to these species with crop an for crop and for of the genetic regulation of traits contributing to waterlogging of an to an ROL barrier to roots of wheat is the wide hybridization of with wheat to produce and et al., et al., a root ROL barrier was in some of a from an not the root ROL barrier trait et al., et al., more is nicaraguensis in maize and traits to waterlogging have in these and is on the tight ROL barrier formation in roots of a trait in maize (Fig. and et al., 2012). The that a tight ROL barrier formation in adventitious roots (Fig. and et al., is an development toward a understanding of root trait and for the to it into maize via The was from the of and was so is needed to develop for use in of root for which is as as to in the of the The use of and plants to specific with using the oxygen Methylene Blue by quantitative using oxygen by et and enable the of the in knowledge of the root ROL barrier In waterlogged soils, the root system can suffer from a of oxygen, and the resulting low as aerenchyma is present (Bailey-Serres and Voesenek, adventitious roots, are from the in to root functioning (i.e. water and as as and Voesenek, 2013; and 2016). water occurs during deeper adventitious roots also can from the of the The of and ethylene in tissues can the signaling for adventitious root in many (Visser and Voesenek, et al., and in (e.g. et al., rice has as a to the signaling that results in the growth of adventitious roots from that are constitutively at The essential of ethylene in adventitious root from of rice and a from the root tip to the in in the death of the cells the root tip et al., 2012). Moreover, the of is in the signaling of cell death et al., 2012). and a on signaling and the formation of adventitious roots in to stress. root formation is by genetic at as the of root root and adventitious root formation have in and and the have elsewhere et al., 2014). Many species to soil by the of an increased number of adventitious roots. for adventitious root formation have in maize et al., Zea mays ssp. et al., and nicaraguensis et al., These mapping populations produced from maize and from maize and mays ssp. or a mapping produced from maize and for adventitious root formation by soil (i.e. the water a waterlogged were on and et al., on and et al., and on and et al., of between mapping populations indicated that some et al., mapping populations produced from the cucumber greater adventitious root and the adventitious analysis was to the adventitious root formation during soil waterlogging et al., The increased adventitious root formation under waterlogged soil conditions were on and analysis that within the of the on were in to soil waterlogging et al., of the be a for the of adventitious root formation for the The development of or that these with adventitious roots would be a to identify the the of these roots and to further the of adventitious root formation for waterlogging of these two plants often to floods resulting in shoot by of adventitious roots also from the along the in to the basal a is rice et al., These aquatic adventitious roots into the water and nutrients in the and et al., a between the of from the and the of aquatic adventitious roots et al., Moreover, plants that were to form of aquatic adventitious roots and more growth than plants in which the formation of aquatic adventitious roots was et al., The summarized only during and The growth of aquatic adventitious roots in under and not be by oxygen et al., status also the growth of aquatic adventitious roots, but status to be via during et al., to et al., and, thus, Thus, the formation of aquatic adventitious roots depends on as (i.e. part of the is or oxygen of and also latter two during floods resulting in plant adventitious roots also can the internal of the of some with aquatic adventitious roots oxygen in at as to only in roots had et al., 2016). The roots are more than the tissues and a area for to between the plant and the and the adventitious roots are with the via oxygen that from the can into the et al., 2016). aquatic adventitious roots also produce oxygen in et al., on aquatic adventitious adventitious roots can in oxygen status during a In a aquatic adventitious roots of between of of anoxia in the cortex during the by in oxygen upon to at as oxygen was produced by the shoot et al., The in aquatic root oxygen status by were even more in the cortex to in the which during the to as low as just to et al., for plants with adventitious roots in anoxic soil, the tissues in oxygen as for with of anoxia during the and in root oxygen to 14 at during et al., or for the aquatic plant root oxygen between and et al., The on root functioning of these in oxygen status can be (e.g. root only during the when oxygen was and during the when for et al., and further This Update has on root traits of ROL barrier induction, and adventitious research on these traits and Greenway, 2003; Greenway and Gibbs, 2003; Bailey-Serres and Voesenek, 2008; and Voesenek, et al., 2014). on aquatic adventitious roots are and research is needed on and water from the water and on the of these roots in and and oxygen to the of these roots for plants with or Moreover, the on aquatic root functioning of in oxygen status and of radial in oxygen the roots, which can in an anoxic or and further Recent and have important of the signaling pathways in the formation of root induction of a tight ROL barrier, and of adventitious roots. This Update has on in understanding the signaling and genetic regulation of these root but the for research on the of roots of various species to soil and root functioning in and water from waterlogged soils also is et al., 2014). The of a tight ROL barrier, as as root the of on the acquisition of nutrients and water during soil waterlogging and upon the growth of further In to signaling during root acclimation to waterlogging, has in the between and signaling for aerenchyma formation and regulation at the et al., (e.g. these root traits to be with laser microdissection were and many with aerenchyma formation in maize roots et al., Takahashi et al., and tight ROL barrier formation in rice roots et al., were of the to understanding of the the formation of aerenchyma and also of the tight ROL of for root traits are to identify the of the for these in understanding of the that the root traits under soil et have the in nicaraguensis by and of maize with or more for these root and have maize these The in maize nicaraguensis traits for the tight ROL barrier, and adventitious root formation be to the waterlogging of be needed to the of these root traits in various waterlogging-flooding and soil for the maize as as for and genetic of waterlogging in and for some images in also and for and of the