Regulation of adventitious root system architecture in response to flooding in rice (Oryza sativa L.)
Flooding is a severe environmental stress that lowers crop production worldwide. Unlike most other crops, rice is a semi-aquatic plant with high flooding tolerance. The gaseous hormone ethylene accumulates in flooded rice plants and controls a number of adaptive responses. In deepwater rice (Oryza sativa L.), that get highly flooded for several months, ethylene induces internodal elongation and adventitious root (AR) growth. Stem growth helps flooded plants to keep their leaves above the water. In rice, ARs are constitutively formed and emerge at the nodes of flooded plants to replace damaged roots. AR growth is mediated by ethylene that gets trapped inside submerged plant parts and is coordinated with programmed death of epidermal cells that cover root primordia. ARs support or replace the main root system by taking up water, nutrients and oxygen from flood waters and by providing anchorage. The deepwater rice variety C9285 harbours three main quantitative trait loci (QTLs) that confer flooding tolerance. QTL12 includes two group VII ERF (ethylene response factor) transcription factor genes, Snorkel1 (SK1) and Snorkel2 (SK2) that were shown to induce rapid stem elongation. This study showed that QTL12 also promotes AR formation and growth upon submergence. Aside from the typical ARs that form at the node, a second type of ARs develop at the base of the internode and these two types of roots are morphologically different. EIN3-LIKE 1 (OsEIL1) is a transcription factor, that directly targets the SK genes. The overexpression of OsEIL1 in nondeepwater rice plants lacking SK genes shows a minor effect on AR formation and growth indicating that SKs are essential for the enhanced formation of ARs. ROS levels were significantly higher in the near-isogenic line NIL-12 compared with wildtype plants suggesting that Snorkels may mediate AR formation and growth by upregulating the ROS level. In brief, the data revealed a major role for QTL12 in AR development. Naturally, rice plants grow in a light/dark cycle. However, flood water can be turbid thereby reducing underwater light intensity and underwater photosynthesis even in the daytime. Reduced photosynthesis means that less oxygen is produced underwater making oxygen shortage of roots more severe in the dark. We describe that darkness not only alters underwater metabolism but has a profound developmental effect on the root system. In the dark, growth of ARs is induced at stem nodes of deepwater rice with roots growing at an upward angle. A similar AR growth pattern is observed in soil suggesting that this root behaviour is advantageous to the plant. Gravity is one of several environmental factors that are integrated to adjust the angle of root growth which, in turn, determines the soil or water layers that will be explored by these roots. Clinostat experiments revealed that gravity increased the root angle suggestive of an antigravitropic growth component. Red, far-red and blue light induced a negative phototropic response of ARs, with blue light as the most effective light signal. cpt1 (coleoptile phototropism1), a component of phototropin signaling, showed a decreased sensitivity to blue light indicating that phototropin and phytochrome signalling regulate the root system architecture. The AR growth angle is thus controlled genetically and by the environmental cues light and gravity. The auxin transport inhibitor naphthylphtalamic acid (NPA) effectively repressed root emergence. The expression of auxin efflux carrier genes was investigated by using OsPIN:β-glucuronidase reporter lines. OsPIN1b and OsPIN1c were active in the root cap and root stele suggestive of a role in root development. OsPIN2 was specifically expressed in epidermal cells above the root primordia and at a lower level in the root tip indicating a role for polar auxin transport in AR emergence. Auxin activity as detected with the DR5:VENUS reporter increased in the root primordia during AR emergence and decreased in epidermal cells above ARs that undergo programmed cell death prior to AR emergence. The results indicate that local auxin gradients determine emergence, growth rate and growth direction of ARs revealing a deep impact of controlled auxin transport on the overall architecture of the AR system.
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