The Wild Sugarcane and Sorghum Kinomes: Insights Into Expansion, Diversification, and Expression Patterns

Alexandre Hild Aono,Gabriel Rodrigues Alves Margarido,Ana Letycia Basso Garcia,Lucas Borges Dos Santos,Danilo Augusto Sforça,Marishani Marin Carrasco,Welison Andrade Pereira,Thiago Willian Balsalobre,Melina Cristina Mancini,Marcos Gonçalves Quiles,James Shiniti Nagai,Cláudio Benício Cardoso-Silva,Marcos Guimarães De Andrade Landell,Anete Pereira De Souza,Guilherme Kenichi Hosaka,Monalisa Sampaio Carneiro,Fernando Henrique Correr,Ricardo José Gonzaga Pimenta,Luciana Rossini Pinto

doi:10.3389/fpls.2021.668623

Abstract

The protein kinase (PK) superfamily is one of the largest superfamilies in plants and the core regulator of cellular signaling. Despite this substantial importance, the kinomes of sugarcane and sorghum have not been profiled. Here, we identified and profiled the complete kinomes of the polyploid Saccharum spontaneum (Ssp) and Sorghum bicolor (Sbi), a close diploid relative. The Sbi kinome was composed of 1,210 PKs; for Ssp, we identified 2,919 PKs when disregarding duplications and allelic copies, and these were related to 1,345 representative gene models. The Ssp and Sbi PKs were grouped into 20 groups and 120 subfamilies and exhibited high compositional similarities and evolutionary divergences. By utilizing the collinearity between the species, this study offers insights into Sbi and Ssp speciation, PK differentiation and selection. We assessed the PK subfamily expression profiles via RNA-Seq and identified significant similarities between Sbi and Ssp. Moreover, coexpression networks allowed inference of a core structure of kinase interactions with specific key elements. This study provides the first categorization of the allelic specificity of a kinome and offers a wide reservoir of molecular and genetic information, thereby enhancing the understanding of Sbi and Ssp PK evolutionary history.

Highlights

Sugarcane is one of the world’s most important crops, with the highest production quantity and the sixth highest net production value in 2016 (FAO, 2020)
Similar to other kinomes (Singh et al, 2014; Wei et al, 2014; Zulawski et al, 2014; Liu et al, 2015; Yan et al, 2017, 2018; Zhu et al, 2018a,b), the most abundant group in both species was the receptor-like kinase (RLK)-Pelle group (Figure 1), which accounted for ∼70% of the PKs, followed by the calcium- and calmodulinregulated kinase (CAMK); cyclin-dependent kinase, mitogenactivated protein kinase, glycogen synthase kinase, and cyclindependent kinase-like kinase (CMGC); tyrosine kinase-like kinase (TKL); serine/threonine kinase (STE); and cyclic AMP-dependent protein kinase, cGMP-dependent protein kinase, and lipid signaling kinase families (AGC); and casein kinase 1 (CK1) groups
Sorghum bicolor (Sbi) was found to belong to a cohesive clade with Zea mays (Zma), Brachypodium distachyon (Bdi), and Sbi v.1, and Saccharum spontaneum (Ssp) belonged to a clade with Setaria italica (Sit) and Oryza sativa (Osa)

Summary

Introduction

Sugarcane is one of the world’s most important crops, with the highest production quantity and the sixth highest net production value in 2016 (FAO, 2020). This crop has accounted for approximately 80% of the worldwide sugar production (ISO, 2020) and is predicted to account for nearly 40% of the planet’s first-generation biofuel supply in the near future (Lalman et al, 2016) It is known for its unprecedented genomic complexity; modern cultivars arose from interspecific crosses between two autopolyploid species, namely Saccharum officinarum (2n = 8x = 80, x = 10; D’Hont et al, 1998) and the wild Saccharum spontaneum (2n = 5x =40 to 16x = 128; x = 8; Panje and Babu, 1960). Due to both the evolutionary proximity between the two species and the extensive collinearity between their chromosomes, sorghum has historically been considered a diploid model for sugarcane (Grivet and Arruda, 2002)

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