An integrated analysis of transcriptome and metabolome provides insights into the responses of maize (Zea mays L.) roots to different straw and fertilizer conditions

Abstract

Returning straw back to the field with an appropriate amount of fertilizer has been proven to be beneficial in the promotion of soil fertility, crop yield, and the sustainability of an agricultural system. However, little is known regarding the molecular and metabolic understandings of enhanced crop growth in a straw return system. By performing an integrated transcriptomic and metabolomics analysis, we investigated the effects of straw removal and straw return with two chemical fertilizer rates on root morphology in a mesh bag field experiment on maize in northwest China. Our results showed that straw return played a role in root thickening (bigger root diameter), while fertilization enhanced root branching (more root number). Different from straw return alone, straw return with fertilizer significantly decreased the root/shoot ratio ( p < 0.01) and increased the total root number ( p < 0.01), and root total nitrogen concentration ( p < 0.001). Root morphological responses were tightly associated with transcriptional regulation (e.g., root dry weight, Mantel’s r = 0.6468, p < 0.001) and metabolism modulation (e.g., root/shoot ratio, Mantel’s r = 0.7229, p < 0.001), mainly including the activation of genes related to phenylpropanoid and flavonoid metabolic pathways (e.g. , BGLU , PAL and POD ), the fine regulation of genes associated with auxin synthesis, homeostasis, flow and signaling (e.g., YUC , AUX1 and SAUR ), and cell wall remodeling (e.g., CESA and EXPA ), and the regulation of transcription factors and genes that function in the development of roots (primary, seminal, and lateral), root hairs, root tips, and root caps (e.g., BBM , LRP1 and RTCS ), and the accumulation of different metabolites (e.g., indole, esculin, and sucrose) under straw return with fertilization. We revealed important insights into the growth-promoting and morphology-modifying effects of straw return, as well as its highly novel effects on the transcriptional regulation and metabolism reprogram of maize root, which may help to elucidate how maize roots respond under straw return conditions to optimize soil resource acquisition and then guide the suitable utilization of crop residue resources in the agricultural system. • Straw played different roles from fertilizer in maize roots morphological modification. • Root growth response to straw was tightly associated with transcriptional regulation. • Genes related to IAA synthesis, homeostasis, flow and signaling were fine-regulated. • R/T ratio showed the strongest Mantel’s correlate with metabolism modulation. • Mechanism governing the enhanced maize growth in a straw-return system was revealed.