The Physiology of Adventitious Roots

Abstract

Adventitious roots are plant roots that form from any nonroot tissue and are produced both during normal development (crown roots on cereals and nodal roots on strawberry [Fragaria spp.]) and in response to stress conditions, such as flooding, nutrient deprivation, and wounding. They are important economically (for cuttings and food production), ecologically (environmental stress response), and for human existence (food production). To improve sustainable food production under environmentally extreme conditions, it is important to understand the adventitious root development of crops both in normal and stressed conditions. Therefore, understanding the regulation and physiology of adventitious root formation is critical for breeding programs. Recent work shows that different adventitious root types are regulated differently, and here, we propose clear definitions of these classes. We use three case studies to summarize the physiology of adventitious root development in response to flooding (case study 1), nutrient deficiency (case study 2), and wounding (case study 3).

Figure 1.

Examples of adventitious root types. This figure highlights a few examples of the diversity of adventitious roots. A to D show types of adventitious roots that form during normal development, including those potentially established in the embryo (A); the dominant root system of monocots, including maize (top image) crown roots (yellow) and brace roots (orange) and nodal roots on other grasses (bottom image; B) and on eudicots such as strawberry (C); and nonnodal roots that provide support for plants such as ivy (top image) and mangroves (bottom image; D). E to H show adventitious root development under stressed conditions: Arabidopsis under low or no light (used as a model for adventitious root regulation; E); burial (top image) or flooding (bottom image) can induce adventitious roots from either nodal or nonnodal stem positions (F); nutrient or heavy metal stress increases adventitious root development (G); and wounding such as cutting induces de novo adventitious root development (H). Primary and seminal roots are depicted in white, first order lateral roots in blue, and second order lateral roots in pink.

Figure 2.

Adventitious root development in response to flooding. Under aerated conditions, gaseous ethylene escapes from plant tissues, but during flooding, water acts as a physical barrier, trapping ethylene in the plant. GA enhances the ethylene-promoted adventitious root growth, while abscisic acid reduces the effect. Ethylene triggers reactive oxygen species production, and together they trigger epidermal programmed cell death for root emergence and cortical programmed cell death lysigenous aerenchyma formation. The main difference in some eudicots (e.g. tomato) is the requirement for de novo adventitious root initiation via auxin and ethylene signaling. In the cross section, epidermis and exodermis are combined, but the exodermis can be several cell layers adjacent to the epidermis. Yellow roots are adventitious roots, blue and pink roots are lateral roots, and white roots are primary roots. Pointed arrows represent positive interactions, and flat-ended arrows represent negative interactions.

Figure 3.

Nutrient responses in adventitious roots. Under nutrient-replete conditions, crown roots have the lowest nutrient uptake rates, followed by seminal roots, while the primary roots have the highest uptake. When nutrients are deficient, the expression of nutrient transporters increases. In addition, strigolactone increases while auxin decreases, resulting in long roots with minimal lateral roots. Reactive oxygen species increase via changes in antioxidant enzyme activity (catalase, superoxide dismutase, and peroxidase) and, together with enhanced ethylene sensitivity, trigger lysigenous aerenchyma formation. When nutrients are replaced, nutrient transporter expression decreases systemically, cytokinin production increases, strigolactone levels decrease, and lateral root initiation increases on the adventitious roots. In potassium and zinc deficiency-tolerant lines, auxin signaling increases, and in potassium-efficient lines, cytokinin signaling decreases, together resulting in more adventitious roots. In phosphorus-efficient lines, more adventitious roots are found in the surface layers of the soil. In the cross section, epidermis and exodermis are combined, but the exodermis can be several cell layers adjacent to the epidermis. Pointed arrows represent positive interactions, and flat-ended arrows represent negative interactions. –K, Potassium deficiency; –P, phosphorus deficiency; –Zn = zinc deficiency. Yellow roots are crown roots, orange roots (the upper, short ones here) are brace roots (both adventitious root types), cream roots are seminal roots, white roots are primary roots, and blue and pink roots are lateral roots. ACC, 1-Aminocyclopropane-1-carboxylic acid (an ethylene precursor).

Figure 4.

Adventitious root formation on cuttings. In intact plants, cytokinin and strigolactones are predominantly produced in the root, while auxin is predominantly produced in the shoot. On wounding, jasmonic acid peaks within 30 min and is required for successful root development. Reactive oxygen species, polyphenols, and hydrogen sulfide also increase and promote adventitious rooting. Polyphenols do this via reducing auxin degradation. Auxin builds up in the base of the cutting, acting upstream of nitric oxide to promote adventitious root initiation. Auxin, nitric oxide, and hydrogen peroxide (H₂O₂) increase soluble sugars, which can be used for root development. Furthermore, levels of root initiation inhibitors (cytokinin and strigolactone) are reduced with the removal of the original root system. At later stages, auxin inhibits primordia elongation while ethylene promotes adventitious root emergence. As the new root system establishes, the production of cytokinin and strigolactones is restored. Pointed arrows represent positive interactions, and flat-ended arrows represent negative interactions. Yellow roots are adventitious roots, the white root is a primary roots, and blue roots are lateral roots.