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The Rhizosheath – a Potential Trait for Future Agricultural Sustainability Occurs in Orders Throughout the Angiosperms

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The Rhizosheath – a Potential Trait for Future Agricultural Sustainability Occurs in Orders Throughout the Angiosperms Plant Soil DOI 10.1007/s11104-017-3220-2 REGULAR ARTICLE The rhizosheath – a potential trait for future agricultural sustainability occurs in orders throughout the angiosperms Lawrie K. Brown & Timothy S. George & Konrad Neugebauer & Philip J. White Received: 21 December 2016 /Accepted: 6 March 2017 # Springer International Publishing Switzerland 2017 Abstract when root hairs were extremely short, but the presence Aims The rhizosheath is defined as the weight of soil of root hairs was required for rhizosheath formation. adhering strongly to roots on excavation, and current Conclusions The rhizosheath is present in species from interest in this trait as a potential tolerance mechanism to many angiosperm orders. Potential to enhance the trait is abiotic stress has prompted us to explore the extent of its likely to exist in a range of crop species and could help occurrence throughout the angiosperm phylogeny. contribute to future agricultural sustainability. Methods Here we describe a robust, novel method which was used to screen species for the presence/absence and Keywords Rhizosheath . Angiosperm phylogeny. strength of a rhizosheath. We correlate the latter with root Root hairs . Agricultural sustainability. Abiotic stress hair length to provide insight into some of the factors tolerance . Second green revolution affecting its formation. We go on to compare experimen- tal data with previous observations in the literature. Results Results of a glasshouse screen demonstrate that rhizosheaths exist in species from many angiosperm Introduction orders, and the frequency of their occurrence and their strength and size are related. No correlation between It is now well over 100 years since the root feature, root hair length and rhizosheath size was found, except known today as the rhizosheath, appeared in the litera- ture (Volkens 1887) with early research into its form being conducted on samples of desert grasses collected by botanists of the time, including Arthur Tansley (Price Responsible Editor: Hans Lambers. 1911). Until recently, the limited research into this be- lowground trait has focused mainly on its structure, Electronic supplementary material The online version of this article (doi:10.1007/s11104-017-3220-2) contains supplementary formation and function. material, which is available to authorized users. Originally described as a Bpeculiar sheath, composed : : : of agglutinated particles of sand^ (Volkens 1887), today L. K. Brown T. S. George (*) K. Neugebauer it is defined operationally as the weight of soil that P. J. White The James Hutton Institute, Dundee DD2 5DA, UK adheres strongly to roots on excavation (George et al. e-mail: [email protected] 2014). Its formation and composition is complex and associated with many factors, including root hair length, P. J. White density and morphology (Haling et al. 2010), root and King Saud University, Riyadh 12372, Saudi Arabia microbial mucilage (Watt et al. 1993; McCully 1999; K. Neugebauer Barre and Hallet 2009; Albalasmeh and Ghezzehei University of Nottingham, Loughborough LE12 5RD, UK 2014), soil water content (Watt et al. 1994; Ghezzehei Plant Soil and Albalasmeh 2015), soil texture (Haling et al. 2014), population, and the rhizosheath could have an important mycorrhizal fungi (Moreno-Espindola et al. 2007)and role in a Second Green Revolution (Lynch 2007). free-living bacteria (Unno et al. 2005). While there has been considerable research into the Various functions of the rhizosheath have been sug- rhizosheaths of desert grasses, in which they were first gested. Price (1911) proposed rhizosheaths to be a observed (Price 1911;Buckley1982; Goodchild and mechanism for improving drought resistance and the Myers 1987;Danin1996a;Othmanetal.2004), and protection of roots under arid conditions, and more some research in other grass species (Duell and Peacock recent research supports this hypothesis (Pate and 1985;BaileyandScholes1997; Bergmann et al. 2009), Dixon 1996; Shane et al. 2010;Benardetal.2016). In the restriction of rhizosheath research to species within addition to its role in protecting the root from drought the Poales has led to the misconception that rhizosheaths and heat stress, the rhizosheath has potential importance are confined to this order (Duell and Peacock 1985). in coping with other abiotic stresses. These include There has been some research into the rhizosheath in nutrient deficiencies like phosphorus (Brown et al. cereal species including wheat, barley and maize (Watt 2012; Haling et al. 2013), zinc (Nambiar 1976) and et al. 1994; Young 1995; Czarnes et al. 2000;Haling nitrogen (Wullstein 1991;Danin,1996a;Othmanetal. et al. 2013, 2014; Delhaize et al. 2012;Georgeetal. 2004), and stresses associated with soil acidity (Haling 2014) and other monocotyledons, such as rushes (Shane et al. 2010; Delhaize et al. 2012) and soil strength et al. 2009, 2010, 2011), but only a few studies have (Haling et al. 2013, 2014; Albalasmeh and Ghezzehei been performed on a wider range of plants. These in- 2014). Rhizosheaths are effective in alleviating such clude studies on some eudicotyledonous species such as stresses because they provide and maintain good contact cacti (McCully 1999), soybean (Sprent 1975), lupin at the interface of the root and the soil which is essential (Unno et al. 2005) and fig (North and Nobel 1997). for nutrient and water uptake (North and Nobel 1997). McCully (1999) acknowledges the presence of Root hairs, which are tubular shaped cells specialised rhizosheaths on the fine roots of some legumes and a for nutrient uptake (Jungk 2001), enmesh soil particles few eudicotyledonous crop plants, but these have not around the root (Bristow et al. 1985)andareessential been investigated further. The literature suggests that the for the formation of rhizosheaths (Haling et al. 2010; rhizosheath is limited to a discrete range of species Brown et al. 2012). Correlations have been found be- which are adapted to stressful environments. This study tween root hair length and rhizosheath weight, but they will challenge this preconception. vary in strength depending on plant species. In wheat, In a recent study, Smith et al. (2011) performed a global root hair length and rhizosheath weight are strongly survey of the rhizosheath trait in a phylogenetic context correlated (Delhaize et al. 2012), while in barley there using field-grown and herbarium specimens, to produce a is a weaker correlation (George et al. 2014), suggesting phylogenetic map of the trait in the Haemodoraceae fam- that factors other than root hair length are important in ily (Commelinales order). The authors concluded that the determining rhizosheath weight. rhizosheath is probably an ancestral trait for the Recent studies of the rhizosheath have attempted to Haemodoraceae family which is associated with a large gain an understanding of the genetics of the trait in crop degree of phylogenetic conservatism and some secondary plants and quantitative trait loci (QTL) for rhizosheath loss. While such detailed information is helpful in build- weight and relative rhizosheath weight have been iden- ing a picture of the heritability of the trait at family level, tified in barley (George et al. 2014) and wheat (Delhaize no studies to date have attempted to investigate the extent et al. 2015; James et al. 2016). Many of the major of the occurrence of the rhizosheath trait across the whole cereals (wheat, maize, barley, oats, rye and sorghum) angiosperm phylogeny. The bias towards the study of arid form rhizosheaths (Duell and Peacock 1985). Under- grasses and the patchy information on other species means standing the genetics behind this belowground trait we do not have a clear picture of the extent of this trait may provide plant breeders with genetic markers to among angiosperms. improve the ability of other species of crop plants to In addition, there is no consensus methodology for deal with environmental variability and abiotic stress. determining the presence, or measuring the strength, of This understanding has importance for improved agri- rhizosheaths. Much of the historical data pertaining to cultural sustainability in the context of future climate the rhizosheath are based on subjective observation and change, finite resources, and an increasing global anecdotal evidence. The subjective interpretation of the Plant Soil term Brhizosheath^ means that the extent of the research methodology and broaden the extent of the study. The into this trait may be underestimated. For example, combined data have then been mapped onto an abridged many studies into the microbiology of the rhizosphere phylogenetic tree at order level. might actually be studies of the rhizosheath (Bulgarelli et al. 2012). Baily and Scholes (1997)alsonotethatthe strength of bonding of the rhizosheath differs between Materials and methods species, with the rhizosheaths of some species being more easily removed than those of other species, sug- Glasshouse screen gesting that variation exists in rhizosheath type or form. Here we describe a simple, quick and environmen- An objective method for assaying the presence/ tally robust method for screening a broad range of absence and strength of the rhizosheath was devel- agriculturally and horticulturally relevant species to es- oped for glasshouse-grown plants and used to score tablish the frequency (presence/absence) and strength of 58 species in 19 orders of angiosperms (Table 1). the rhizosheath across the angiosperm phylogeny. In Four replicates of each species were pre-germinated
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