Tissue-specific auxin signaling in response to temperature fluctuation

Abstract

Auxin levels are well regulated in cells and tissues by both transport and local biosynthesis, and its distribution is important for the modulation of cell proliferation, differentiation, development, tropisms and high-temperature response. Activation of auxin biosynthesis with increased temperatures reported in certain plant tissues. In contrast, our studies indicated that male tissue-specific auxin reduction via transcriptional repression of the YUCCA auxin biosynthesis genes is the primary cause of high temperature injury, which leads the abortion of pollen development in Arabidopsis and barley Hordeum vulgare L. Furthermore, the abortion can be reversed by the application of exogenous auxin, suggesting that the application may maintain crop yields during the current global warming crisis.

Phytohormones are signaling molecules that regulate various aspects of plant growth, development, differentiation and adaptation. The phytohormone auxin is essential for the modulation of many processes including cell proliferation, development, phototropism, gravitropism, hydrotropism, apical dominance, senescence and cell specificity.¹ The shoot apical meristem (SAM) is responsible for generating all the aerial parts of a plant including the floral meristem, and auxin plays a key role in meristem activities. Regulation of the auxin distribution pattern in meristem tissues is performed by the auxin transporter families, PIN^2,3 and AUX (auxin influx carrier),¹ as well as by local and tissue-specific auxin biosynthesis.⁴

Efflux carriers transport auxin from cell to cell in a polar manner. One such carrier, PIN1, was first identified in an Arabidopsis mutant that exhibited a pin-formed phenotype.² PIN1 is a member of the PIN protein family, which provide directional auxin transport in response to various endogenous and environmental signals.³

Auxin IAA biosynthesis occurs mainly via a tryptophan-dependent pathway that includes four parallel and partially-interdependent pathways.^5,6 The YUCCA (YUC) family of auxin synthetic genes encode flavin monooxygenases, which are involved in an pathway that produces IAA via the intermediate indole-3-acetaldoxime (IAOx).⁷ The Arabidopsis YUC family comprises 11 members and double, triple and quadruple mutant combinations display strong inflorescence and floral developmental defects, as well as alterations to leaf vasculature.⁸ The expression patterns of certain YUCCA genes are controlled spatially and temporally in developing anthers.^8–10 Ikeda et al.¹¹ have indicated that in root tips, auxin biosynthesis occurs through expression of the anthranilate synthase, and it contributes to generation of a homeostatic gradient and local activation of auxin signaling. Thus, regulation of auxin levels in cells and tissues is achieved by both transport and local biosynthesis of auxin, and the distribution of auxin is important for transcriptional control of differentiation and development.^1,12

Although plants can grow over a broad range of temperatures, exposure to high temperatures (HT) results in dramatic changes to development, including rapid extension of plant axes, leaf hyponasty and early flowering.^13,14 In Arabidopsis, HT promotes auxin-mediated elongation of hypocotyls.¹³ In hypocotyls, cotyledons and roots, HT-induced elongation requires upregulation of the tryptophan aminotransferase-encoding gene TAA1/TIR2A, which is involved in one of the auxin biosynthetic pathways.^15–17 CYP79B2 and CYP79B3, Arabidopsis cytochrome P450s involved in pathways that synthesize auxin via IAOx, have also been shown to play roles in hypocotyl elongation.¹⁸ Recently, Koini et al.¹⁹ demonstrated that HT-induced architectural adaptations are mediated by the bHLH transcriptional regulator PIF4. Thus, PIF4-deficient mutants do not exhibit HT-induced elongation responses, leaf hyponasty or auxin-responsive gene IAA29 upregulation. These results suggest that PIF4 responds to temperature signaling by interacting with the auxin response via biosynthesis.¹⁹

In some plant species, male reproduction is particularly susceptible to environmental stress and HT stress can cause significant injury during anther development.²⁰ Thus, the recent global warming trend represents a threat to plant reproduction processes. Lobell and Field²¹ have reported a negative correlation between increased temperatures and worldwide yields of wheat, maize and barley. They estimate that for these crops alone, global warming has resulted in an annual combined loss of approximately 40 megatons, or $5 billion, per year since 1981.

HT increases auxin levels in many tissues.^13,17–19 However, we demonstrated that HT upregulates expression of certain auxin-repressed proteins in barley panicles, which suggests that HT mediates depletion of auxin in reproductive tissues.²² In fact, HT conditions reduce endogenous auxin levels and auxin activity in the developing anthers of barley and Arabidopsis (Fig. 1).²³ Increasing temperatures also repress expression of Arabidopsis YUC2, YUC6 and barley homologs.²³ Interestingly, the mutant phenotypes of Arabidopsis double or triple mutants of yuc2 and yuc6, are quite similar to the injuries observed in male reproductive development following HT stress. Specifically, these mutants completely lose male fertility and form short stamens that lack pollen grains.⁸ We observed that increased temperatures amplify auxin signals at the top of the gynoecium and around the vascular cells of petals in Arabidopsis (Fig. 1), as well as in rachis cells around the vascular bundles of developing barley panicles.²³ However, HT treatment clearly represses auxin signaling in an anther cell-specific manner, leading to abortion of pollen development and filament elongation. In both Arabidopsis and barley, the application of exogenous auxin can reverse abortion of pollen development and male sterility. Since a reduction in male tissue-specific auxin appears to be the primary result of HT injury in monocots and dicots, auxin treatment may be useful for promoting plant fertility and maintaining crop yields during the current global warming crisis.²³ Surprisingly, decreasing temperatures have the opposite effect on anther cells, which respond by increasing auxin signaling activities (Fig. 1). These findings lead to the conclusion that tissue-specific auxin signaling is a finely modulated response to temperature fluctuation, and that it is controlled using the auxin transport system and local biosynthesis.

Figure 1.

Temperature affects DR5-GUS expression in developing Arabidopsis anthers at stage 10. Flowering transgenic Arabidopsis DR5-GUS plants were cultured at 23°C and then transferred to growth cabinets at 10 or 31°C. After 24 h exposure to different temperatures, floral apices were dissected and stained for β-glucuronidase activity.

Abbreviations

GUS

β-glucuronidase

HT

high temperature

IAOx

indole-3-acetaldoxime

SAM

shoot apical meristem

Addendum to: Sakata T, Oshino T, Miura S, Tomabechi M, Tsunaga Y, Higashitani N, et al. Auxins reverse plant male sterility caused by high temperatures. Proc Natl Acad Sci USA. 2010;107:8569–8574. doi: 10.1073/pnas.1000869107.