Transcriptomic and anatomical complexity of primary, seminal, and crown roots highlight root type-specific functional diversity in maize (Zea mays L.).

Huanhuan Tai,Frank Hochholdinger,Andrew Lithio,Dan Nettleton,Caroline Marcon,Nina Opitz,Xin Lu,Anja Paschold

doi:10.1093/jxb/erv513

Huanhuan Tai, Frank Hochholdinger + Show 6 more

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https://doi.org/10.1093/jxb/erv513

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Abstract

Maize develops a complex root system composed of embryonic and post-embryonic roots. Spatio-temporal differences in the formation of these root types imply specific functions during maize development. A comparative transcriptomic study of embryonic primary and seminal, and post-embryonic crown roots of the maize inbred line B73 by RNA sequencing along with anatomical studies were conducted early in development. Seminal roots displayed unique anatomical features, whereas the organization of primary and crown roots was similar. For instance, seminal roots displayed fewer cortical cell files and their stele contained more meta-xylem vessels. Global expression profiling revealed diverse patterns of gene activity across all root types and highlighted the unique transcriptome of seminal roots. While functions in cell remodeling and cell wall formation were prominent in primary and crown roots, stress-related genes and transcriptional regulators were over-represented in seminal roots, suggesting functional specialization of the different root types. Dynamic expression of lignin biosynthesis genes and histochemical staining suggested diversification of cell wall lignification among the three root types. Our findings highlight a cost-efficient anatomical structure and a unique expression profile of seminal roots of the maize inbred line B73 different from primary and crown roots.

Highlights

Roots play a vital role in plant development and fitness because they provide mechanical support, mediate water and nutrient uptake from soil, and interact with microbial communities in the rhizosphere
The analysis revealed that enriched or under-represented categories among genes preferentially expressed in primary (K1+K2+K3) or crown roots (K7+K8+K9) were relatively similar, whereas genes preferentially expressed in seminal roots (K4+K5+K6) displayed distinct enrichment patterns
Primary and shoot-borne roots are formed in all cereal species, while seminal roots are present in maize (Robertson et al, 1979), wheat (Erdelska and Vidovencova, 1993), and barley (Luxová, 1986), but not in rice (Morita and Abe, 1994), sorghum (Singh et al, 2010), and the grass model species brachypodium (Watt et al, 2009)

Summary

Introduction

Roots play a vital role in plant development and fitness because they provide mechanical support, mediate water and nutrient uptake from soil, and interact with microbial communities in the rhizosphere (reviewed in Hawkes et al, 2007; Zhu et al, 2011; Villordon et al, 2014). 1124 | Tai et al. The root stock of maize consists of an embryonically formed primary root and a variable number of embryonic seminal roots and post-embryonic shoot-borne crown and brace roots (reviewed in Feldman, 1994; Hochholdinger et al, 2004a, b). The root stock of maize consists of an embryonically formed primary root and a variable number of embryonic seminal roots and post-embryonic shoot-borne crown and brace roots (reviewed in Feldman, 1994; Hochholdinger et al, 2004a, b) These root types are initiated from distinct tissues during successive stages of development. In the first weeks after germination, primary and seminal roots make up the major portion of the seedling root stock (Hochholdinger et al, 2004b) and are vital for the early vigor of young maize seedlings (Peter et al, 2009). A commonality of all major embryonic and post-embryonic root types is their ability to initiate post-embryonic lateral roots from pericycle and endodermis cells (Fahn, 1990)

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